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

Abstract

In both humans and rodents, maternal care is disturbed by exposure to environmental adversity, including low resource conditions (i.e., poverty, scarcity). Maternal adversity is associated with compromised quality of mother-infant attachment and increased adverse caregiving patterns such as abuse, maltreatment and/or neglect), which disrupt behavioral development in the female offspring. Importantly, maternal behavior is thought to be an intergenerational behavior, meaning that the quality of maternal care a female experiences during early life is thought to influence the quality of care she will display towards her own offspring when she becomes a mother. Here, we tested this idea by employing a rodent model of postpartum environmental adversity based on creating an impoverished nesting environment during postpartum days (PD) 2–9, which disrupts mother-infant interactions and is thought to upregulate hypothalamic-pituitary-adrenal (HPA)-axis function in the pups. We examined the impact of this form of early life adversity on pup stress hormone (i.e., corticosterone- CORT) levels by collecting trunk blood and later life maternal behavior by conducting maternal behavior observations and maternal motivation tests (e.g., T-Maze, pup retrieval, pup-associated conditioned place preference) in the first filial (F1) generation. We report no impact of early life scarcity-adversity/adverse caregiving on pup CORT levels or later life naturalistic or motivated maternal behaviors. In sum, we show that female rat pups who experienced adverse caregiving during early life showed resilience towards developing negative caregiving patterns, as they did not perpetuate the same aberrant maternal behavior that they received from their mothers.

Introduction

The swift onset of maternal behavior following parturition is evolutionarily conserved in humans and other altricial mammals, as it is advantageous to species 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 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 both intergenerational transmission of abusive parenting (Maestripieri, 2005) as well as an enhancement in 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 due to 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 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 levels 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.

Methods

Animals

All animals used were housed in ventilated cages on a 12-h light/dark cycle (6AM lights on/6PM lights off) with ad libitum access to food and water. Adult (PND 70–90) virgin female Sprague-Dawley rats (obtained from Inotiv, Indianapolis, IN) were bred in house using standard procedures. Breeding entailed cohousing a female with an adult male breeder for a 3-week period after which the pregnant female was separated and single-housed. Parturition was verified daily (2–3x per day) from gestational days 20–23 and the day of birth was designated as postpartum day (PD) 0 (for dams) and postnatal day (PND) 0 (for pups). On PD/PND 2, all litters were culled to 10 pups with equal sex distribution (5 males, 5 females) whenever possible and simple randomization (i.e. coin flip) was used to assign dams to control or experimental (i.e., scarcity-adversity) conditions. Virgin female rats that were obtained from Inotiv and bred in house were classified as first-generation parent (F0) dams and experienced scarcity-adversity from PD 2–9. To examine the impact of early life scarcity-adversity on later life maternal behaviors, two female offspring per litter were weaned on PND 23 and cohoused in sex-matched pairs in standard conditions (i.e., ~1800 ml of corncob bedding and a nestlet) until adulthood. Adult female offspring (F1) were bred in-house as described above (see Figure 1, Experimental Design and Timeline). Notably, F1 dams and their F2 pups did not experience scarcity-adversity during their postpartum or postnatal days, respectively, as they were housed in standard conditions (i.e., ~1800 ml of corncob bedding and a nestlet). A total number of 123 rats were used for these experiments. This number includes 10 F0 CON dams, 10 F0 ADV dams and the number of F1 and F2 progeny used for the study. To control for litter effects, only 1 rat per litter was used for any measure evaluated. All experiments were carried out according to NIH guidelines and were approved by the University of Texas at Dallas Institutional Animal Care and Use Committee.

Fig. 1. Experimental Design and Timeline.

A) F0 dams consisted of adult female rats that were originally obtained from Inotiv and bred in house. Two of the female offspring (i.e., F1 generation) were kept past weaning and matured into adults. At PN 80–90, these F1 female offspring were bred to produce pups (i.e., F2 generation). B) Experimental timeline of the F0 dam and F1 pups who experienced control or scarcity-adversity conditions from PD/PND 2–9. C) Experimental timeline of F1 observation dams who experienced control or scarcity-adversity conditions as neonates and underwent maternal behavior observations. D) Experimental timeline of a subset of F1 dams who experienced control or scarcity-adversity conditions as neonates then underwent a series of behavioral tests during postpartum to assess maternal motivation. Figure created with BioRender.com

Scarcity-adversity paradigm

The scarcity-adversity paradigm implemented here consisted of reducing the amount of bedding and nesting materials available to the dam from PD 2–9 (Lauraine et al., 2024; Rincon-Cortes and Grace, 2022b). This environmental manipulation leads to changes in pup-directed maternal behaviors and constitutes a form of postpartum adversity for the dam (F0) and, consequently, early life adversity for the pups (F1) (Gilles et al., 1996; Ivy et al., 2008; Rincon-Cortes and Grace, 2022b; Walker et al., 2017). Litters assigned to the scarcity-adversity condition received 500 mL of corncob bedding and no nesting material whereas control litters received 1800 mL of corncob bedding and a nestlet (Lauraine et al., 2024). Both control and scarcity-adversity groups remained in their respective conditions until PD/PND 9 after which all groups were housed in standard conditions (i.e., ~1800 mL of corncob bedding and a nestlet).

Maternal observations

Both F0 and a subset of F1 dams (i.e., F1 Observation Dams, see Figure 1) underwent 30-minute maternal observation sessions twice daily (i.e., morning, afternoon) from PD 2–5 in which maternal behaviors were closely monitored within the home cage (standing <1 foot away). This range (i.e., PD 2–5) was selected for maternal observations based on prior literature highlighting these days as having robust behavioral effects (Lauraine et al., 2024; Rincon-Cortes and Grace, 2022b). Maternal behaviors scored included: time spent in nest, nursing, licking, anogenital licking, nest-building, stepping on pups, dragging pups (i.e., pups nipple attached while dam moves around the cage), shoving pups (i.e., dam using head or paws to push pups away), transporting pups (i.e., dam picks pup up with their mouth and relocates them away/out of nest), and biting/chasing tail- a stress-related behavior in rodents (Kubo et al., 2015).

To score maternal behaviors, each 30-minute observation session was divided into 5-minute segments during which behaviors were scored as occurring or not. To do this, dams were spot-checked periodically during each 5-minute segment and if a behavior occurred during that segment, a tally mark was made. To represent behaviors as a percentage of time, we divided the number of segments in which the behavior was observed by the total number of observation segments on all days (Lauraine et al., 2024; Porras et al., 2024; Rincon-Cortes and Grace, 2022b). Maternal observation calculations were done by a different experimenter (other than the one who recorded the maternal observations) that was blinded to the dam’s experimental condition.

Weight Assessment

To determine if there was an impact of scarcity-adversity on maternal weight in the F0 generation as well as dam and pup weights in the F1 generation, we recorded weights on PD/PND 2 and PD/PND 9 (Table 1). The average weight of pups per litter was calculated for each sex.

Table 1. Effect of scarcity-adversity on F0 and F1 dam weights, F1 and F2 pup weights, and F1 and F2 pup CORT levels.

Mean ± standard deviation (SD) is shown for numerical variables.

Weights (g)	PD/ PND 2
		Male			Female
	CON	ADV	p value	CON	ADV	p value
F0 Dams	---	---	---	278.1 ± 15.35	277.0 ± 20.98	p = 0.89
F1 Pups	8.51 ± 0.83	8.16 ± 0.96	p = 0.40	8.09 ± 0.95	7.85 ± 0.81	p = 0.55
F1 Dams	---	---	---	289.5 ± 14.96	295.4 ± 21.59	p = 0.54
F2 Pups	8.38 ± 1.32	7.7 ± 0.61	p = 0.23	7.93 ± 1.11	7.29 ± 0.7	p = 0.21
Weights (g)	PD/ PND 9
		Male			Female
	CON	ADV	p value	CON	ADV	p value
F0 Dams	---	---	---	297.6 ± 18.40	284.4 ± 20.44	p = 0.15
F1 Pups	23.06 ± 1.64	20.37 ± 1.34***	p = 0.0008	22.12 ± 1.73	19.3 ± 1.24***	p = 0.0006
F1 Dams	---	---	---	319.3 ± 3.08	311.5 ± 20.59	p = 0.38
F2 Pups	21.55 ± 2.5	22.68 ± 2.22	p = 0.39	20.68 ± 2.33	21.46 ± 1.41	p = 0.47
CORT (ng/mL)	PND 9
		Male			Female
	CON	ADV	p value	CON	ADV	p value
F1 Pups	7.69 ± 3.13	9.39 ± 2.43	p = 0.19	5.53 ± 1.53	5.16 ± 1.91	p = 0.64
F2 Pups	7.76 ± 3.24	6.31 ± 2.77	p = 0.37	5.24 ± 2.49	4.73 ± 1.48	p = 0.64

^***p < 0.001.

Trunk Blood Collection and Serum Extraction

To test the hypothesis that early life scarcity-adversity programs later life maternal behavior via HPA-axis dysregulation (Champagne and Meaney, 2001; Francis and Meaney, 1999), we collected pup trunk blood in F1 PND 9 pups (1 male, 1 female per litter) to assess whether early life scarcity-adversity resulted in atypical infant increases in basal pup CORT levels. In addition, to probe for potential transgenerational effects on basal CORT levels, we also collected trunk blood in F2 PND 9 pups (1 male, 1 female per litter). All animals were decapitated from 8:00 am- 10:00 am within 1 minute of being removed from their cage to minimize stress artifacts on basal CORT measurements (Gartner et al., 1980). Trunk blood was collected in a 2 mL microcentrifuge tube and placed on ice immediately until all samples were collected. Samples were then allowed to sit at room temperature and coagulate for 1 hour after which they were centrifuged for 15 minutes at 4°C, 3200 rpm (Porras et al., 2024). The resulting supernatant (serum) was aliquoted into 0.5 mL SafeLock centrifuge tubes and stored at −80°C until further use.

CORT Assay

Serum concentrations of CORT were determined using a CORT ELISA kit according to the manufacturer’s instructions (Enzo Life Sciences Co., Farmingdale, New York). The sensitivity of this kit is 26.99 pg/mL (0.03 ng/mL) for CORT. ELISA plates were read on a microplate reader (accuSkan FC. ThermoScientific) which yielded optical density values used to create a four-parameter logistic curve on GraphPad Prism 10.1.2. Sample concentrations were interpolated from this curve, and standard dilution accuracy was validated by reverse interpolating the standards’ optical density values into concentrations and comparing these to the expected standard concentrations. Additionally, a coefficient of variance percentage (%CVs) was calculated for each sample replicate. In accordance with the manual, the average intra-assay %CV for low concentrations (i.e., 171 pg/mL) was 8.0% or less and for high concentrations (i.e., 780 pg/mL), was 6.6% or less. Likewise, the average inter-assay %CV for low concentrations (i.e., 174 pg/mL) was 13.1% or less and for high concentrations (i.e., 780 pg/mL), was 7.8% or less. CORT concentrations are reported here in ng/mL.

Behavioral testing

To determine the impact of early life scarcity-adversity on later life maternal motivation, a subset of F1 dams (i.e., F1 Behavior Dams) underwent a series of behavioral tests from PD 6–12 (see Figure 1D). These tests sought to assess aspects of maternal motivation including pup approach, pup retrieval (PR), and conditioned place preference (CPP) for a pup-associated chamber. Behavior tests were conducted in the following order: T-Maze (PD 6), PR (PD 8), and CPP (PD 9–12). All testing occurred between 11:00 AM– 4:00 PM during the animal’s light cycle under normal light. All animals were allowed to habituate to the behavior room for 30 minutes prior to any test or conditioning day. All behavioral apparatus were cleaned with 70% ethanol in between animals. All tests were recorded with an overhead video camera and later scored with an automated behavioral tracking software (i.e., ANY-Maze), by a blinded experimenter. Behaviors that could not be scored with ANY-Maze (i.e., latency to retrieve pup in T-Maze and PR tests) were hand scored by an experienced scorer that was blinded to the animal’s experimental condition.

T-Maze:

The T-Maze test is based on the innate tendency rodents have to explore their environment and obtain natural rewards with minimum effort (Trezza et al., 2011). Here, we used the T-Maze test to examine maternal approach responses to pups (Rincon-Cortes and Grace, 2020). On PD 6, dams were tested for pup approach (i.e., the latency to reach pup arm), pup retrieval behavior (i.e., latency to retrieve pup from pup arm and move it to another arm/center), and locomotor behavior (i.e., the total distance traveled) during a 10-minute test. The test consisted of placing one pup at the end of the left or right arm and releasing the dam into the maze from the start arm. Each test was counterbalanced using a male or female pup and alternating the arm in which the pup was placed in (i.e., right or left) to control for any sex or place preferences. The latency to reach the pup arm and the total distance traveled were scored using ANY-Maze, and the latency to retrieve the pup was hand scored.

Pup Retrieval:

The PR test is commonly used to measure goal-directed maternal responses and motivated maternal behavior (Rincon-Cortes and Grace, 2020, 2022b). On PD 8, dams underwent one PR test consisting of a 5-minute habituation to the apparatus (which also served as a brief separation from the pups) and a 10-minute test (Rincon-Cortes and Grace, 2022b). Briefly, this test consisted of placing four pups into the apparatus, one in each corner in their own ramekin containing some home cage bedding. Dams were tested for pup retrieval behavior (i.e., the latency to retrieve the first pup from their ramekin and move it to another corner or into the center), pup retrieval efficacy (i.e., the percentage of pups the dam retrieved), and locomotor activity (i.e., total distance traveled). The latency to retrieve the first pup and percentage of pups retrieved were hand scored, and total distance traveled were scored using ANY-Maze.

Conditioned Place Preference:

The CPP test is typically used to measure the rewarding value of different stimuli (Tzschentke, 1998, 2007), and has been previously adapted to assess the rewarding aspect of pups to dams (Fleming, 1994; Mattson et al., 2001; Pereira and Morrell, 2010; Wansaw et al., 2008). We adapted the CPP test to assess how early life scarcity-adversity affects the rewarding properties of pup-related contexts in dams. The CPP apparatus consisted of two side chambers providing different visual and contextual cues (i.e., one dotted chamber, one lined chamber) so that the rats could distinguish between the two and a smaller, center chamber. The CPP procedure was carried out on consecutive days from PD 9–12: one preconditioning day (PD 9), two conditioning days (PD 10 and PD 11), and one test day (PD 12). On the preconditioning day, dams were habituated to the CPP apparatus by being placed in the center chamber and were allowed to roam freely for 10 minutes during which the amount of time the dam spent in each chamber was recorded to determine which chamber the dam preferred (if any). Using the baseline chamber preference determined during preconditioning, the dams were then conditioned for two consecutive days so that their preferred chamber was empty (henceforth referred to as the control chamber), and the less-preferred chamber contained their pups (henceforth referred to as the pup chamber). This counterbalanced design was done to ensure that any change in chamber preference was due to the conditioning and not to pre-existing chamber preferences. On each conditioning day, the dam was placed in the control chamber with no other stimuli (i.e., no pups) for 30 minutes, which also served as a brief separation from the pups known to induce a burst in positive maternal behaviors upon reunion with the litter (Bodensteiner et al., 2012). During this time away from the dam, pups were kept warm using a heating lamp. Immediately after the conditioning session to the control chamber, the dam was placed in the opposite chamber, which contained their entire litter and some nesting material for one hour. Previous studies have shown that two one-hour conditioning sessions with their pups is sufficient time to establish a pup chamber association (Fleming, 1994; Sarkisova et al., 2016). To ensure that the dam adequately associates the chamber with pups, we observed maternal care behaviors (i.e., nursing or licking) during the last 15–20-minute of their conditioning time. Following the two conditioning days, dams underwent a 10-minute test in which they were allowed to freely roam the CPP apparatus (in the absence of pups), and the time spent in each chamber was recorded.

Preconditioning and test days were recorded with an overhead video camera and later scored with an automated behavioral tracking software (i.e., ANY-Maze) by a blinded experimenter. Total time spent in the pup chamber on test day, pup chamber preference (i.e., [time spent in pup chamber/total test time] × 100), and the change in pup chamber preference (i.e., % preference during test – % preference during preconditioning) were scored. In this test, the time rat spends in the chambers with the pup-associated cues indicates the motivation or desire for the pup stimulus in its absence (Mattson and Morrell, 2005). Thus, an increase in time spent in the pup chamber or pup chamber preference suggests that the dam successfully formed an association between the conditioned chamber and her pups and implies normal maternal motivation and salience of pup cues (Wansaw et al., 2008).

Statistical Analysis

Data sets with a normal distribution were analyzed using unpaired two-tailed t-tests; data sets deviating from the normal distribution (as indicated by not passing the Shapiro-Wilk test) were analyzed using Mann–Whitney U tests. Statistics were calculated using GraphPad Prism 10.1.2 and differences were considered significant at p < 0.05. Statistical outliers were identified using the robust regression and outlier removal (ROUT) method with Q=1% (GraphPad Prism) and excluded from analysis. For behavioral testing, 2 animals were excluded from ADV group in the pup retrieval test because they were identified as statistical outliers using the ROUT method. No animals were excluded from the T-Maze or the CPP tests.

Results

Effects of postpartum scarcity-adversity on maternal behaviors in F0 dams

Dams exposed to postpartum scarcity-adversity exhibited altered maternal behaviors compared to control dams (Figure 2). Compared to control dams (n=7–10), scarcity-adversity dams (n=10) exhibited an increased percentage of time spent in the nest (U = 1, p < 0.0001), nursing pups (t₁₈ = 2.87, p = 0.01), licking pups (t₁₈ = 2.32, p = 0.03), but no differences in anogenital licking of pups (t₁₈ = 2.08, p = 0.05) (Figure 2A–D). Compared to control dams, scarcity-adversity dams spent more time nest building (t₁₈ = 6.16, p < 0.0001) (Figure 2E). Scarcity-adversity dams also exhibited increased percentages of time spent stepping on pups (U= 5, p = 0.0002), dragging pups (t₁₈ = 5.20, p < 0.0001), shoving pups (U = 0, p < 0.0001), and transporting pups (U = 4, p = 0.0003)(Figures 2F–I). Moreover, scarcity-adversity exposed dams spent more time biting or chasing their tails (U = 5, p = 0.0001) compared to control dams (Figure 2J). For mean standard deviation values per group and summary statistics, please see Supplementary Figure S1.

Figure 2. Effects of scarcity-adversity on maternal behaviors in the F0 generation.

A) Compared to control (CON) dams, scarcity-adversity (ADV) dams spent a higher percentage of time in the nest (p < 0.0001). B) ADV dams exhibited an increased percentage of time nursing pups (p = 0.01). C) ADV dams exhibited an increased percentage of time licking pups (p = 0.03). D) ADV dams displayed comparable percentage of time engaged in anogenital licking of pups (p = 0.05). E) ADV dams exhibited an increased percentage of time spent building or re-building her nest (p < 0.0001). F) ADV dams exhibited an increased percentage of time stepping on pups (p = 0.0002). G) ADV dams exhibited an increased percentage of time dragging pups (p < 0.0001), H) ADV dams exhibited an increased percentage of time shoving pups (p < 0.0001). I) ADV dams exhibited an increased percentage of time transporting pups around the home cage (p = 0.0003). J) ADV dams exhibited an increased percentage of time biting or chasing her tail (p = 0.0001). Error bars represent mean ± SEM. Black dots represent control group (n = 7–10), and blue squares represent the experimental (ADV) group (n = 10). * p < 0.05, ** p < 0.01, *** p < 0.001, **** p < 0.0001.

No impact of scarcity-adversity on F0 maternal body weight

There was no weight difference between control or scarcity-adversity dams (n=10 per group) on PD 2 (t₁₈ = 0.13, p = 0.89) or PD 9 (t₁₈ = 1.52, p = 0.15)(see Table 1 for mean, standard deviation values and summary statistics), suggesting no impact of postpartum scarcity-adversity on maternal weight gain.

Early life scarcity-adversity reduces F1 pup weight at PND 9 without altering pup CORT levels

To determine whether early life scarcity-adversity disrupted pup weight or HPA-axis activity, we assessed pup weight on PND 2 and PND 9 and collected trunk blood to measure serum CORT levels in F1 generation on PND 9 (see Table 1 for mean, standard deviation values and summary statistics). On PND 2 (i.e., prior to the onset of scarcity-adversity), no differences in pup weight were found between the control or scarcity-adversity groups (n=10 per group) for males (t₁₈ = 0.87, p = 0.40) or females (t₁₈ = 0.61, p = 0.55). However, scarcity-adversity did significantly decrease male (t₁₈ = 4.01, p = 0.0008) and female (t₁₈ = 4.19, p = 0.0006) pup weights on PND 9 when compared to their control counterparts, suggesting an impact of scarcity-adversity at this age. In males, no differences were found between the control or scarcity-adversity groups for serum CORT levels on PND 9 (t₁₈ = 1.35, p = 0.19). In females, no differences were found between the control or scarcity-adversity pups (n=10 per group) for serum CORT levels on PND 9 (t₁₈ = 0.47, p = 0.64).

No effects of scarcity-adversity on maternal behaviors in the F1 generation

To assess the effects of early life scarcity-adversity on later life caregiving behaviors, we conducted maternal observations from PND 2–5 in the adult female offspring of F0 dams (i.e., the F1 generation, n=7–9 per group) (Figure 3). No significant differences were observed between the control or scarcity-adversity offspring for time spent in the nest (t₁₆= 1.87, p = 0.08), nursing (t₁₆ = 1.73, p = 0.10), licking pups (t₁₆ = 1.01, p = 0.33), anogenital licking of pups (t₁₆ = 0.65, p = 0.52), nest building (t₁₆ = 0.11, p = 0.91), stepping on pups (U = 20.5, p = 0.30), dragging pups (U = 28, p = 0.28) shoving pups (U = 28, p > 0.9999), transporting pups (U = 36, p = 0.71), or biting or chasing their tails (U = 40.5, p > 0.9999)(Figures 3A–J). For mean and standard deviation values per group and summary statistics, please see Supplementary Figure S2.

Figure 3. Effects of scarcity-adversity on maternal behaviors in the F1 generation.

A) Control (CON) and scarcity-adversity (ADV) F1 dams spent a comparable percentage of time in the nest (p = 0.08). B) CON and ADV F1 dams spent comparable percentages of time nursing pups (p = 0.10). C) CON and ADV F1 dams exhibited comparable percentages of time spent licking pups (p = 0.33). D) CON and ADV F1 dams spent comparable percentages of time spent engaged in anogenital licking of pups (p = 0.52). E) CON and ADV F1 dams spent comparable percentages of time nest building (p = 0.91). F) CON and ADV F1 dams exhibited comparable percentages of time stepping on pups (p = 0.30). G) CON and F1 ADV dams exhibited comparable percentage of time dragging pups (p = 0.28). H) CON and ADV F1 dams exhibited comparable percentages of time shoving pups (p > 0.9999). I) CON and ADV F1 dams exhibited comparable percentages of time transporting pups (p = 0.61). J) Neither control nor scarcity-adversity dams spent time biting or chasing their tails (p > 0.9999). Error bars represent mean ± SEM. Black dots represent control group (n = 7–9), and blue squares represent the experimental (ADV) group (n = 8–9).

To determine if there was a difference in the total number of adverse caregiving behaviors towards pups between the control and scarcity-adversity dams from PD 2–5 in the F0 and F1 generation, we tallied all negative maternal behaviors (e.g., transporting pups, dragging pups, stepping on pups, shoving pups) to render the total number of occurrences across all observation periods from PND 2–5 (Figure 4). This approach has been used by previous studies examining maternal behaviors following ELA and is thought to provide more resolution that can been lost when collapsing behaviors across time bins (Keller et al., 2019; Murgatroyd and Nephew, 2013). In the F0 generation (n=10 dams per group), scarcity-adversity dams exhibited an increased number of occurrences in adverse caregiving behavior towards pups (t₁₈ = 5.62, p < 0.0001) compared to the control dams (Figure 4A). In the F1 generation, both groups (i.e. CON and ADV, n=9 per group) exhibited a comparable number of occurrences in adverse caregiving behaviors towards pups (U = 33.5, p = 0.56)(Figure 4B). For mean and standard deviation values per group and summary statistics, please see Supplementary Figure S3. In sum, F0 dams exposed to postpartum scarcity-adversity displayed more adverse caregiving behaviors compared to control dams; however, F1 dams exposed to early life scarcity-adversity did not exhibit increased adverse caregiving compared to controls.

Figure 4. Effects of scarcity-adversity on total incidences of adverse maternal behaviors in the F0 and F1 generation.

A) In the F0 generation, the scarcity-adversity (ADV) dams exhibited an increase in total adverse caregiving behaviors compared to control dams (p < 0.0001). B) In the F1 generation, both CON and ADV dams exhibited a comparable number of occurrences in adverse maternal behaviors (p = 0.56). Error bars represent minimum to maximum values. White bars with dots represent the control group (n = 10), and blue bars with squares represent the experimental (ADV) group (n = 10). **** p < 0.0001.

No impact of early life scarcity-adversity on F1 maternal body weight

To determine if early life scarcity-adversity influenced weight gain in F1 dams (i.e., adult female offspring of F0 dams), we recorded and compared weights from both the control and scarcity-adversity groups on PD 2 and 9 (see Table 1 for mean, standard deviation values and summary statistics). Dams previously exposed to early life control or scarcity-adversity conditions (n=6–8 per group) had comparable weights on PD 2 (t₁₃ = 0.62, p = 0.54) and PD 9 (t₁₁ = 0.92, p = 0.38).

No effect of early life scarcity-adversity on weight or CORT levels in F2 pups at PND 9

To determine if early life scarcity-adversity influenced weight gain in the progeny of F1 dams (i.e., F2 pups), we recorded and compared weights from both the control and scarcity-adversity groups on PND 2 and 9 (see Table 1 for mean, standard deviation values and summary statistics). The male progeny (F2, n=7–8 per group) of F1 control and scarcity-adversity dams also had comparable weights on PND 2 (t₁₃ = 1.24, p = 0.23) and PND 9 (t₁₂ = 0.89, p = 0.39). The female progeny (F2, n=7–8 per group) of F1 control and scarcity-adversity dams also had comparable weights on PND 2 (t₁₃ = 1.3, p = 0.21) and PND 9 (t₁₂ = 0.75, p = 0.47).

To determine whether early life scarcity-adversity disrupted HPA-axis activity in the progeny of F1 dams, we collected trunk blood to measure baseline serum CORT levels on PND 9 (see Table 1 for mean, standard deviation values and summary statistics). In males (n=7–8 per group), no differences were found between control or scarcity-adversity serum CORT levels in F2 pups (t₁₃ = 0.92, p = 0.37). In females (n=7–8 per group), no differences were found between control or scarcity-adversity serum CORT levels in F2 pups (t₁₃ = 0.47, p = 0.64).

No impact of early life scarcity-adversity on maternal motivation or pup reward in F1 dams

To evaluate early life scarcity-adversity changes in maternal motivation and/or pup reward, both control and scarcity-adversity adult female offspring (i.e., F1 dams, n=8–9 per group) underwent a series of behavioral tests (e.g., T-maze, PR, CPP)(Figure 5). In the T-maze, control and scarcity-adversity dams showed comparable latencies to reach the pup arm (t₁₆ = 1.06, p = 0.30) retrieve pups (U = 37, p = 0.79), and total distance traveled (U = 39, p = 0.93)(Figures 5A–C). In the PR test, control and scarcity-adversity dams showed comparable latencies to retrieve the first pup (U = 17, p = 0.13), percent of pups retrieved (U = 30.50, p = 0.37), and distance traveled (t₁₆ = 1.83, p = 0.08), (Figures 5D–F). In the CPP, there were no between group differences for time spent in pup chamber (t₁₆ = 0.42, p = 0.68), pup chamber preference score (t₁₆ = 0.24, p = 0.81), or percent change from baseline (i.e. preconditioning) to test (t₁₆ = 1.206, p = 0.24)(Figures 5G–I). For mean and standard deviation values per group and summary statistics, please see Supplementary Figure S4.

Figure 5. No impact of early life adversity on later life maternal motivation/pup reward.

A) Control (CON) and scarcity-adversity (ADV) F1 dams exhibited comparable latencies to reach the pup arm of the T-Maze (p = 0.30). B) CON and ADV F1 dams exhibited comparable latencies to retrieve pups (p = 0.79) in the T-Maze. C) CON and ADV F1 dams exhibited similar distances traveled in the T-Maze (p = 0.93). D) CON and ADV F1 dams exhibited comparable latencies to retrieve their first pup in the PR test (p = 0.13). E) CON and ADV F1 retrieved comparable percentages of pups (p = 0.37). F) CON and ADV F1 dams traveled comparable distances during the PR test (p = 0.08). G) CON and ADV F1 dams exhibited comparable times spent in the pup chamber during the CPP test (p = 0.68). H) CON and ADV F1 dams exhibited comparable pup chamber preference scores in the CPP test (p = 0.81). I) CON and ADV F1 dams exhibited similar percent change from baseline for the pup-associated chamber of the CPP (p = 0.24). Error bars represent minimum to maximum values. White bars with dots represent the control group (n = 8–9), and blue bars with squares represent the experimental (ADV) group (n = 7–9).

Discussion

In this study, scarcity-adversity was implemented either during the early postpartum [i.e., PD 2–9 (F0 dams)] or early life [i.e., PND 2–9 (F1)] and maternal behavior was evaluated in two generations (i.e., F0 and F1 dams). Additionally maternal motivation was assessed in second-generation (i.e., F1) dams. Postpartum scarcity-adversity conditions induced aberrant maternal behaviors that impacted F1 progeny weight gain on PND 9 but did not increase their basal CORT levels. Consistent with this lack of infant HPA axis hyperactivity, which was hypothesized to program later life behavior, we did not observe any subsequent aberrant maternal behavior in F1 dams who experienced scarcity-adversity and aberrant caregiving during early life. Furthermore, these F1 dams did not show deficient maternal motivation or impaired pup reward across behavioral tests (e.g., T Maze, PR, or CPP). Finally, neither F1 dams nor their progeny (i.e., F2 pups) exhibited scarcity-adversity-induced weight differences, and F2 pups did not have elevated basal CORT levels compared to controls. These findings are discussed below.

Postpartum scarcity-adversity alters pup-directed maternal behaviors in the rat dam

Postpartum scarcity-adversity has been shown to induce aberrant patterns of maternal care, including increases in adverse pup-directed behaviors in rodents that mimic maltreatment (Blaze et al., 2013; Ivy et al., 2008; Keller et al., 2019; Raineki et al., 2012; Rincon-Cortes and Grace, 2022b). In agreement with past studies, the present study found increased percentages of stepping on pups, dragging pups, shoving pups, improper transport of pups, and nest-building in F0 dams who experienced scarcity-adversity from PD 2–9 compared to control dams (Blaze et al., 2013; Rincon-Cortes and Grace, 2022b; Roth et al., 2009; Shupe and Clinton, 2021). However, F0 dams also showed increases in other maternal behaviors such as increased time spent in the nest, as well as higher percentages of nursing and licking pups. This increase in sensitive caregiving has been reported by other groups and is thought to be compensatory for an inadequate nesting environment that may reflect a scarcity-adversity-induced hypervigilant dam (Eck et al., 2020; Gallo et al., 2019). Interestingly, a recent study showed that scarcity-adversity exposure alters several pup cues known to modulate maternal behavior, including reducing pup core body temperature, altering pup vocalizations, and elevating circulating testosterone levels in pups (Lapp et al., 2024). These alterations are thought to influence maternal behaviors such as nursing behaviors, nest attendance, as well as licking and grooming bouts (Lapp et al., 2024). Thus, it is possible that alterations in these pup cues may be eliciting distinct patterns of maternal care behaviors. In addition, F0 dams also displayed significant increases in chasing and biting their tail, a stress-coping behavior that has been previously reported in rat dams exposed to resource scarcity (Lauraine et al., 2024; Shupe and Clinton, 2021). Finally, it is worth mentioning that a limitation of the current work is that some maternal behaviors (e.g., shoving, improper transport and tail chasing and/or biting) were not observed at all in control dams (i.e., they exhibited 0 instances of the behavior and thereby 0 percentage of time). The presence of excessive zeros in the distribution of the control group could result in zero-inflation and possible overdispersion of the data, and thereby inflated Type I errors (Perumean-Chaney et al., 2013). We could not fit our data into a zero-inflated model given that we did not have a large enough sample size, which based on previous work would be around an n=50 (Perumean-Chaney et al., 2013). However, the presence of statistical differences for shoving, transport and tail chasing and/or biting behaviors between CON and ADV dams suggests no Type I errors and is consistent with previously published work showing that postpartum exposure to scarcity-adversity increases these behaviors (Lauraine et al., 2024; Rincon-Cortes and Grace, 2022b).

Exposure to scarcity-adversity had no impact on F0 and F1 rat dams but decreased F1 pup weight on PND 9

Although we found no impact of scarcity-adversity on maternal weight in F0 or F1 dams, we found short-term consequences of aberrant maternal caregiving in the progeny of F0 dams (i.e., F1 pups), which had significant weight differences on PND 9 (i.e., the last day of the scarcity-adversity paradigm). Indeed, male and female pups exposed to early life scarcity-adversity weighed significantly less than their control counterparts on PND 9, despite scarcity-adversity dams spending more time nursing. This is consistent with previous literature reporting differences in pup weights following early life resource scarcity and aberrant maternal caregiving (Brunson et al., 2005; Eck et al., 2020; Lapp et al., 2024; McLaughlin et al., 2016; Moussaoui et al., 2016; Shupe and Clinton, 2021). Others have postulated that this significant weight difference in scarcity-adversity pups despite the increase in nursing suggests that scarcity-adversity affected the quality of maternal care rather than the quantity of maternal care (Eck et al., 2020), which is consistent with a prior study showing that pups reared under scarcity adversity conditions have reduced levels of micronutrients (Naninck et al., 2017). However, our results showing no weight differences in F1 adult female offspring during the postpartum (i.e., when they become F1 dams) may suggest that effects of early life resource scarcity on weight are not long-lasting.

Early life scarcity-adversity did not alter basal CORT levels on PND 9 in F1 or F2 pups

Previous studies have found increased CORT levels in rat pups who have experienced early life resource scarcity from PND 2–9 (Avishai-Eliner et al., 2001; Brunson et al., 2005; Gilles et al., 1996). In contrast, this study found no differences in PND 9 F1 or F2 male or female pup basal CORT levels compared with controls, suggesting that our adapted scarcity-adversity paradigm does not upregulate HPA-axis activity in pups at this time-point. This is consistent with a previous study showing no differences in serum CORT levels in scarcity-adversity pups on PND 6 or PND 10 (Lapp et al., 2020). There could be multiple factors contributing to these discrepancies regarding the impact of early life resource scarcity on pup CORT levels. First, the limited bedding and nesting (LBN) paradigm employed by the Baram lab also includes the use of a wire mesh floor, which could serve as an extra stressor that is sufficient to upregulate HPA-axis activity in pups at this age (~PND 9) (Avishai-Eliner et al., 2001; Brunson et al., 2005; Gilles et al., 1996). Second, other labs employing the scarcity-adversity paradigm (without including the use of a wire mesh floor) during later time points (i.e., PND 8–12) have reported increases in basal CORT levels at PND 12–13 (Perry et al., 2020; Raineki et al., 2019). Taken together, these findings may suggest that the combination of resource scarcity and the wire mesh floor is necessary to induce an increase in pup CORT levels prior to PND 10 and that the timing of the scarcity-adversity paradigm is important for increasing pup CORT levels, as scarcity-adversity alone (in the absence of the wire mesh floor) from PND 8–12 is sufficient to increase pup CORT levels. In addition, the timing of the CORT measurement may be critical for detecting differences in the offspring. For example, it is possible that there are no changes in basal CORT levels on PND 9, but changes in basal CORT levels might emerge as pups exit the stress-hyporesponsive period. Indeed, a previous study conducted in male and female LBN mice found no differences in basal CORT levels between LBN and control mice prior to PND 16, but both LBN males and LBN females exhibited increased basal CORT levels compared to their control counterparts on PND 21 (Demaestri et al., 2020). Thus, a future direction for this study could be to include multiple timepoints for assessing for basal CORT levels across early development (i.e., before and after the stress hyporesponsive period).

Considering that early life scarcity-adversity did not increase baseline pup CORT levels in the F1 or F2 generation, our results suggest limited impact of early life scarcity-adversity from PND 2–9 on basal HPA-axis function on PND 9, which is consistent with previously published work (Lapp et al., 2020). Of note, studies examining pup CORT levels following early life resource scarcity in response to acute stressors have found divergent effects (Gilles et al., 1996; McLaughlin et al., 2016). In response to cold separation stress, pups exposed to resource scarcity exhibited a greater increase in plasma CORT levels (Gilles et al., 1996). However, in response to immobilization stress, pups exposed to early life resource scarcity exhibited blunted CORT responses (McLaughlin et al., 2016). Thus, future studies may wish to further examine the impact of early life scarcity-adversity on pup HPA-axis function and regulation by testing CORT responses to a variety of acute stressors in rat pups of both sexes.

No impact of early life scarcity-adversity on later life maternal behaviors

In this study, we evaluated the impact of early life scarcity-adversity on later life mothering by breeding adult F0 progeny (i.e., F1 pups who experienced scarcity-adversity from PND 2–9) and examining the maternal behavior they displayed towards their own litter. Surprisingly, F1 dams exposed to early life scarcity-adversity did not exhibit alterations in maternal behaviors compared to controls, suggesting that exposure to early life scarcity-adversity and disrupted caregiving had no impact on subsequent maternal behavior. This is a novel finding that contrasts with previous studies reporting aberrant and/or deficient caregiving behaviors following several forms of ELA (Carini and Nephew, 2013; Keller et al., 2019; Lovic et al., 2001). For example, dams that experienced maternal separation during early life (PND 1–17) exhibit deficient maternal care during adulthood, as indexed by reduced licking and crouching over pups (Lovic et al., 2001). In a similar vein, dams that were exposed to deficient caregiving during early life (PND 2–16) due to chronic social stress also exhibit alterations in maternal care, as indexed by longer durations of pup retrieval as well as reductions in pup licking, nursing and total maternal care (Carini and Nephew, 2013). With regards to scarcity-adversity, previous studies have shown an increase in the total number of adverse caregiving events in F0 dams exposed to resource scarcity as well as their adult female offspring (F1) when they become mothers (Keller et al., 2019; Roth et al., 2009).

In this study, we did observe an increase in positive as well as adverse caregiving behaviors in the F0 dams exposed to scarcity-adversity from PD 2–9 compared to control dams, but no changes in F1 dams that experienced early life scarcity-adversity from PND 2–9 compared to controls. The lack of differences in positive and negative caregiving behaviors in dams exposed to early life scarcity-adversity compared to controls suggests that maternal behavior patterns were not transmitted from the F0 to the F1 generation. This finding is in contrast with previously published studies showing increased adverse caregiving in both F0 and F1 dams exposed to scarcity-adversity (Keller et al., 2019; Roth et al., 2009). Several factors could have contributed to these differences in results. First, the Roth lab uses a cross-foster maltreatment paradigm that exposed pups to adverse caregiving induced by resource scarcity for 30 minutes daily from PND 1–7, which differs from the current paradigm in which pups are kept with their biological mother and are exposed to scarcity-adversity continuously in the home cage from PND 2–9. Second, we assessed maternal behavior in the F1 generation through daily 1-hour sessions from PD 2–5, whereas the Roth lab study assessed maternal behavior during a single 30-minute test on PD 10 (Keller et al., 2019). Thus, it is possible that early life scarcity adversity may influence maternal behavior at other timepoints or in other contexts than the ones examined in this study. Finally, the Roth lab studies used Long-Evans rats whereas the current study used Sprague-Dawley rats, which raises the possibility that effects of early life scarcity-adversity on later life maternal behaviors in rats could be strain-dependent.

Our findings suggesting resilience following ELA in rodents are consistent with a variety of previously published findings in nonhuman primates and humans. In nonhuman primates, mothers who experienced more ELA nursed and carried their offspring more than mothers who experienced less ELA (Patterson et al., 2021). These results suggest that mothers who experienced high levels of ELA demonstrate greater maternal effort, as indexed by more time spent nursing and carrying offspring. Interestingly, despite this greater maternal effort, mothers that experienced high ELA also had greater offspring mortality (Patterson et al., 2021; Zipple et al., 2019). Interestingly, a follow-up study showed that, in female baboons, the effects of ELA on adult offspring mortality were mediated by adult social relationships (Lange et al., 2023). For example, strong social bonds and high social status in adulthood could enhance survival outcomes in ELA-exposed female baboons (Lange et al., 2023). In humans, around 30% of abused and/or maltreated children grow up to become abusive parents themselves (Oliver, 1993). Thus, most adults that experience child maltreatment break this cycle of abuse and maltreatment (Dym Bartlett and Easterbrooks, 2015; Thornberry et al., 2012; Wilkes, 2002). Factors associated with resilience towards perpetuating the cycle of maltreatment in humans include: high levels of social support, safe and secure intimate partner relationships, positive child-infant relationships, and high satisfaction with parenthood, among others (Dym Bartlett and Easterbrooks, 2015; Jaffee et al., 2013; Langevin et al., 2021). In addition, a study investigating whether the timing of maltreatment (i.e., childhood vs adolescence) influences the intergenerational transfer of maltreatment found that maltreatment that is limited to childhood does not significantly increase the odds of maltreatment perpetration (Thornberry and Henry, 2013). However, maltreatment that occurs in adolescence or that begins in childhood and persists into adolescence does. Within this context, it is possible that prolonging the exposure to early life scarcity-adversity or combining early life scarcity-adversity with adolescent stress exposure may increase adverse caregiving in F1 dams.

In summary, here we demonstrate that early life scarcity-adversity did not program or predict later life maternal behavior in female rats, as F1 dams who experienced early life scarcity-adversity and aberrant caregiving as pups displayed resilience in their subsequent maternal behavior. These results suggest the extinction of adverse maternal behaviors in the second generation (F1 dams) and provide novel evidence that experiencing atypical mothering and early life scarcity-adversity does not program subsequent maternal behavior in rats. This lack of intergenerational transmission of maternal behavior may be due to several reasons. First, we observed that F0 dams exposed to scarcity-adversity exhibited increases in both sensitive and adverse caregiving. Thus, it is possible that this increase in sensitive caregiving may have exerted a protective influence and “buffered” against potential effects induced by increased adverse caregiving. Second, early life scarcity-adversity did not alter basal CORT levels in female pups, suggesting no impact of early life scarcity-adversity on basal HPA-axis activity during infancy. Therefore, it is possible that atypical infant increases in CORT are necessary to program aberrant maternal behaviors during later life. Consistent with this idea, a study conducted in rhesus monkeys assessing the relationship between infant stress reactivity and future parenting style found that higher levels of stress-induced cortisol levels during infancy predicted severity of impairments in maternal behaviors (e.g., offspring approaches and leaves, maternal cradling) during adulthood (Wood et al., 2021). Alternatively, it also possible that a “second hit” during adulthood or the postpartum may be necessary to uncover the effects of early life scarcity-adversity on later life mothering (Daskalakis et al., 2012; Nederhof and Schmidt, 2012). Finally, a limitation of this study is that it is possible that scarcity-adversity influenced maternal behavior in a way that was not detected in this study. For example, in the LBN paradigm, the main change in maternal care is an increase in unpredictable and fragmented care, which is assessed by calculating an entropy score (Molet et al., 2016). Since an entropy score was not scored and cannot be scored due to the methods used in this study, we do not know if there was a change in F0 or F1 dam entropy scores.

Early life scarcity-adversity did not alter later life maternal motivation in female rats

Previous papers have shown abnormalities in motivated maternal behavior (i.e., pup retrieval) during conditions of postpartum adversity (Rincon-Cortes and Grace, 2022b; Scarola et al., 2020). This deficit in maternal motivation is thought to reflect deficits in reward-related processing specifically related to the salience of pups (Dulac et al., 2014; Rincon-Cortes and Grace, 2022a). Indeed, one study has found that postpartum scarcity-adversity triggers a hypodopaminergic state in rat dams (Rincon-Cortes and Grace, 2022b). Given these data, the present study sought to examine maternal motivation in F1 dams who experienced early life scarcity-adversity, and consequently aberrant maternal caregiving, as pups. In accordance with the lack of aberrant maternal behavior observed in the second generation (i.e., F1 dams), no differences in maternal motivation (i.e. latency to approach pups, latency to retrieve pups, amount of time spent in pup chamber, and pup chamber preference) were found in any of the behavioral tests. Thus, control and scarcity-adversity exposed F1 dams displayed similar levels of behavior in all measures in all tests. In the T-Maze test, control and scarcity-adversity F1 dams displayed similar latencies to reach the pup arm and to retrieve the pup. In the PR test, control and scarcity-adversity F1 dams displayed similar latencies to retrieve the first pup and had similar pup retrieval efficacy. as indexed by similar percentages of pups retrieved. In the CPP test, control and scarcity-adversity F1 dams displayed a similar amount of time spent in the pup chamber and pup chamber preference percentage. Collectively, these results suggest that experiencing aberrant maternal caregiving due to scarcity-adversity during early life does not alter or predict later life maternal motivation.

Conclusion

The results of this study suggest that the scarcity-adversity paradigm used here reliably induced aberrant maternal behavior when applied during the early postpartum period (i.e., PD 2–9) but not when experienced during early life (i.e., PND 2–9). Importantly, we show that female pups who experienced adverse caregiving during early life showed resilience towards developing aberrant caregiving patterns, as they did not perpetuate the same adverse maternal behavior as their predecessors. Despite experiencing increased maltreatment as pups, dams exposed to aberrant caregiving due to scarcity-adversity stopped the cycle of maltreatment and displayed intact maternal behavior within the home cage and maternal motivation across 3 different tests.