Female rats exposed to early life scarcity-adversity are resilient to later life changes in maternal behavior

The swift onset of maternal behavior following parturition is evolutionarily conserved in humans and other altricial mammals, as it is beneficial to offspring survival (Broad et al., 2006; Lonstein et al., 2015; Rilling and Young, 2014). However, due to its adaptive nature, maternal behavior can be altered in response to the postpartum environment. In humans, exposure to postpartum adversity, including resource scarcity, is associated with lower levels of maternal sensitivity, which refers to a mother's ability to effectively attend to and respond to her child's cues and signals, as well as increased levels of adverse parenting behaviors like maltreatment or abuse (Coulton et al., 1995; Eckenrode et al., 2014; Eisenberger, 1990; Finegood et al., 2016; Kotch et al., 1995; McLoyd, 1990; Webster-Stratton, 1990). Similar patterns of disrupted mother-infant interactions have been found in maternal rodents that experience adversity in the form of postpartum resource scarcity (Blaze et al., 2013; Gallo et al., 2019; Ivy et al., 2008; Lauraine et al., 2024; Perry et al., 2019; Rincon-Cortes and Grace, 2022b; Walker et al., 2017).

Importantly, clinical and preclinical data suggest that early experiences of being mothered can have long-term effects on the quality of mothering the adult female offspring will show towards their own offspring (i.e., progeny) when they grow up (Champagne and Meaney, 2001; Choi et al., 2019; Fleming et al., 2002; Miller et al., 1997; Savage et al., 2019; Tani et al., 2018). Thus, it has been hypothesized that parenting styles, namely negative ones, can be inherited (Berman, 1990; Champagne and Meaney, 2001; Fairbanks, 1989; Fleming et al., 2002; Lomanowska et al., 2017). This alarming notion has prompted several studies in humans, nonhuman primates, and rats that aim to uncover the extent to which experiencing early life variations in maternal caregiving due to individual differences and/or adversity exposure may influence later life caregiving behavior. In humans, poverty, low socioeconomic status, and/or a history of childhood maltreatment is correlated with an increased risk for psychopathology (Bosquet Enlow et al., 2018; Choi and Sikkema, 2016; Goyal et al., 2010; Guintivano et al., 2018; Muzik et al., 2013) and later life adverse caregiving patterns including abuse, maltreatment, and/or neglect (Finegood et al., 2016; Hall et al., 1998; Juul et al., 2016; Lomanowska et al., 2017). However, it is equally important to mention that human psychology is complex and can be shaped by several factors. Because of this, women who have a history of maltreatment are not necessarily predestined to perpetuate the same adverse caregiving behaviors as their predecessors and can end the cycle of abuse (Dym Bartlett and Easterbrooks, 2015; St-Laurent et al., 2019; Wilkes, 2002). In nonhuman primates, there is evidence for the intergenerational transmission of both abusive parenting (Maestripieri, 2005) and enhanced levels of maternal effort (i.e., time spent nursing and carrying infants) following early life adversity (ELA) (Patterson et al., 2021). In rodents, evidence for the intergenerational transmission of maternal behaviors includes the inheritance of high or low amounts of pup licking (Champagne and Meaney, 2001; Champagne et al., 2003; Francis et al., 1999) and adverse caregiving (Keller et al., 2019; Roth et al., 2009).

In rats, ELA in the form of aberrant maternal caregiving has been modeled using the limited bedding and nesting (LBN) and scarcity-adversity paradigms, which can mimic human patterns of fragmented and adverse maternal care (Glynn and Baram, 2019; Perry et al., 2019; Rincon-Cortes, 2025; Rincon-Cortes and Grace, 2022b; Walker et al., 2017). These alterations are thought to be due to the stressful nature of this impoverished home cage environment, which increases levels of the stress hormone corticosterone (CORT) in the dam (Ivy et al., 2008) and is thought to dysregulate hypothalamic-pituitary-adrenal (HPA) axis function in both dam and pups (Gilles et al., 1996; Rincon-Cortes, 2024; Rincon-Cortes and Sullivan, 2014). While there is ample evidence to support that applying these paradigms during the early postpartum induces dysfunctional maternal behavior (Ivy et al., 2008; Raineki et al., 2010; Rincon-Cortes and Grace, 2022b; Walker et al., 2017), there is minimal research on how experiencing scarcity-adversity-induced adverse caregiving during early life affects later life maternal behavior and maternal motivation. To address this gap in knowledge, we evaluated maternal behaviors in dams who experienced scarcity-adversity during the postpartum [i.e., first-generation, parent generation (F0) dams] and in dams who experienced scarcity-adversity during early life [i.e., second-generation, first filial generation (F1) dams]. Assessing F1 dam maternal behavior may provide insights into how experiencing aberrant caregiving during early life might program subsequent maternal behavior. Additionally, we measured F1 pup CORT levels on postnatal day (PND) 9 (i.e., the last day of scarcity-adversity) to test whether an atypical infant increase in baseline CORT was observed, which could potentially serve as a mechanism by which early life scarcity-adversity disrupts later life maternal behavior and maternal motivation in second-generation (i.e., F1) dams.

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