Emotionally, physically, or psychologically traumatizing events that occur during critical stages of development, from the prenatal period through adolescence, are commonly referred to as early-life stressors (ELS) (Brown et al., 2009). ELS can include, but is not limited to, parental neglect and physical, sexual, or verbal abuse. Children lacking stable parent–child relationships are more likely to exhibit social anxiety (Coupland, 2001), aggression (Lee and Hoaken, 2007, Maas et al., 2008, Bland et al., 2018), social withdrawal (Hildyard and Wolfe, 2002, Rubin et al., 2009) and reduced capabilities to process social information (i.e., social cognition) (Rokita et al., 2018) in later years, compared to children with positive parent–child relationships. The sex of an individual can influence the occurrence, severity, and comorbidity of psychosocial disorders later in life (Berkout et al., 2011, Asher et al., 2017, Masi et al., 2021). For example, the prevalence of social anxiety is higher among women than men (Merikangas et al., 2002, Ohayon and Schatzberg, 2010, MacKenzie and Fowler, 2013); however, McLean et al. (2011) did not report a sex difference in the prevalence of social anxiety disorder among men and women. As Asher et al. (2017) pointed out, this discrepancy may be a result of overly conservative statistical methods, potentially obscuring the detection of sex differences.

Additionally, there is a significantly higher comorbidity of generalized anxiety disorder and post-traumatic stress disorder (PTSD) in women with social anxiety disorder (Asher and Aderka, 2018). While it is suggested that social anxiety is more prevalent in women than men (Merikangas et al., 2002, Ohayon and Schatzberg, 2010, MacKenzie and Fowler, 2013), men with social anxiety are more likely to develop comorbid substance dependency and conduct disorder (Asher and Aderka, 2018). This pattern of sex differences is further reflected in the prevalence of conduct disorder, which is 10–15 times more likely to persist into adulthood in males, compared to females (Eme, 2007, Renk, 2008). Age may also mediate these sex-specific behavioral differences. For example, the increased prevalence of mood disorders in women does not emerge until after the onset of puberty (Bale and Epperson, 2015, Rainville and Hodes, 2018). Also, childhood-onset conduct disorder is more common in males, with aggressive behaviors peaking during adolescence (Eme, 2007, Renk, 2008). These findings suggest that assessing social behaviors across different developmental stages, such as infancy, childhood, and adolescence (see Fig. 1), may provide insight into the development of atypical social behaviors. Understanding these developmental stages is necessary, as they mark key periods when children begin forming social connections that are influenced by early experiences. For instance, during infancy, babies learn to interact with their environment and caregivers, while in childhood, peer interactions become more prominent, and social skills become more complex (Bell, 2018, Ghasemi et al., 2021). Taken together, an individual's sex and age may influence their susceptibility to developing atypical social behaviors later in life in response to impaired parent–child relationships.

Sex-specific behavioral impairments in social behaviors following ELS may also accompany structural alterations to the brain, including regions like the prefrontal cortex (PFC), amygdala (AMYG), and hippocampus (HPC) (McCrory et al., 2010, Teicher et al., 2016, Farber et al., 2020). Alterations in these brain regions can exaggerate the risk of developing psychosocial pathologies later in life (Martins et al., 2011, Carr et al., 2013, Mandelli et al., 2015, Herzog and Schmahl, 2018, Schorr et al., 2020).

The use of retrospective and prospective human studies provides insight into how adverse childhood experiences (i.e., ELS) affect later-life behavior (Mathews et al., 2020). Human studies investigating parenting styles (e.g., affectionate, hostile, inconsistent, and controlling) suggest that both the sex of the parent and the parenting style can differentially affect social development in boys and girls (detailed below in Section 2; Braza et al., 2015, Ruiz-Ortiz et al., 2017, Scott et al., 2018). While these studies are informative, human studies have limitations. Questionnaires are often used to assess ELS effects on adult behavior; however, questionnaires do not properly operationalize the different ELS subtypes (e.g., emotional neglect, physical neglect, physical abuse, emotional abuse, sexual abuse), resulting in broad definitions of child neglect and abuse (Mathews et al., 2020). Failure to operationalize these experiences can compromise the construct validity of the questionnaires. Also, most human studies focus on mother–child relationships or do not assess mother- and father-child relationships independently (Featherstone, 2004, Maxwell et al., 2012). This results in limited data on father-child relationships, as the available data are often generalized as parent-offspring interactions (Featherstone, 2004, Maxwell et al., 2012).

Rodent studies are commonly used to investigate the behavioral and neurobiological effects of ELS. Disrupted parent-offspring relationships can induce stress in postnatal rodents. Rodent models of ELS typically use uniparental species (i.e., Rattus and Mus) and focus on manipulating mother-offspring interactions. As a result, several paradigms emerged, including limited bedding and nesting (LBN), maternal deprivation, and prolonged maternal separation (Brunson, 2005, Cui et al., 2006, De la Fuente et al., 2009, Tractenberg et al., 2016). LBN paradigms reduce the nesting material provided to the home cage for 4–14 days during the initial two weeks of the postnatal period (Walker et al., 2017). Maternal deprivation paradigms separate the dam and pups either once for 24 h (h) or twice for 12 h (12 h per deprivation period); this can occur anytime between postnatal days (PND) 1–14 (De la Fuente et al., 2009, Tractenberg et al., 2016). Lastly, prolonged maternal separation often involves the daily separation of the dam from pups on PND 1–14 for 60–480 min (Tractenberg et al., 2016). Studies using these paradigms demonstrate that disrupting the maternal-offspring bond can induce social impairments, with males displaying more significant atypical social behaviors than females (see Table 1, Table 2, Table 3). Additionally, understanding the extent to which ELS paradigms can induce sex-specific impairments is challenging, as the vast majority of available evidence stems from male-only studies or does not assess males and females separately (Will et al., 2017, Garcia-Sifuentes and Maney, 2021).

The exploration of paternal care in biparental rodent species offers additional insights into the effects of disrupted parent-offspring relationships on behavioral and neurobiological outcomes in offspring. Less than 10 % of mammals exhibit paternal care (Kleiman and Malcolm, 1981). Consequently, biparental species are not often used in models of ELS. In biparental rodent species, the sire engages in the same parental behaviors as the dam, except for nursing (Braun and Champagne, 2014, Bales and Saltzman, 2016, Saltzman et al., 2017), yet the dam may provide more consistent care than the sire (Finton and Ophir, 2020). Despite this, the maternal rodent will not increase offspring care to compensate for the loss of the paternal rodent (Gubernick et al., 1993, Ahern, 2009, Helmeke et al., 2009, Tabbaa et al., 2017, Rogers and Bales, 2020, Madison et al., 2022). Offspring reared without paternal care experience less licking, grooming, huddling, pup retrieval, and play-fighting than biparentally-reared offspring (Ahern, 2009, Helmeke et al., 2009, Rogers and Bales, 2020). When biparental species are utilized in ELS studies, father-offspring interactions are often disrupted, resulting in studies on paternal deprivation.

Paternal deprivation studies use biparental species, as males of uniparental rodent species, such as Rattus and Mus, do not typically engage in paternal care (Saltzman et al., 2017). Two types of paternal deprivation paradigms are used: (1) neonatal paternal deprivation (Bales and Saltzman, 2016) and (2) postnatal paternal deprivation (He et al., 2017, He et al., 2018, He et al., 2019). Neonatal paternal deprivation involves permanently separating the paternal rodent from the litter between PND 0–3 (Bales and Saltzman, 2016), while postnatal paternal deprivation studies permanently remove the paternal rodent on PND 14 (He et al., 2017, He et al., 2018, He et al., 2019). Several biparental rodent species are used in paternal deprivation studies, including California mice (Peromyscus californicus), prairie voles (Microtus ochrogaster), mandarin voles (Microtus mandarinus), and degus (Octodon degus). Numerous studies suggest paternal deprivation may induce more significant impairments in females than in males (see Table 4).

Assessing rodent behavior following ELS can be done at various developmental stages (neonatal, infantile, juvenile, adolescence, and adulthood). However, the timing and duration of these stages may vary by species and sex (see Fig. 1), making it challenging for researchers to define them consistently (Brust et al., 2015, Bell, 2018, Ghasemi et al., 2021). The neonatal period, which lasts until PND 6 in Rattus and PND 4 in Mus, is marked by increased vocalizations as pups seek maternal care, peaking during this stage and declining at the onset of infancy (Bell, 2018, Ghasemi et al., 2021). The infantile stage spans PND 7–21 in rats and PND 5–21 in mice; this developmental period begins when pups gain the ability to open their eyes (Bell, 2018, Ghasemi et al., 2021). During this period, infantile uniparental rodents will receive increased sensory input as they begin to explore and interact with their environment more (Smirnov and Sitnikova, 2019). The juvenile stage begins at weaning, when uniparental rodents are artificially weaned by researchers ∼PND 21 (Bechard and Mason, 2010); however, some complex social interactions, like play behavior and alloparental care, may emerge earlier, suggesting the juvenile period may start before PND 21 (Bell, 2018). The juvenile stage ends around the onset of puberty, marked by vaginal opening in females and preputial separation in males; these are species- and sex-specific (Bell, 2018, Ghasemi et al., 2021, see Fig. 1). The adolescent period follows, characterized by pubertal changes and the onset of aggressive behaviors; adolescence is completed by PND 60 in Mus and PND 70 in Rattus, signaling the end of sexual maturation and the start of adulthood (Brust et al., 2015, Bell, 2018, Ghasemi et al., 2021).

Investigations into the onset and duration of developmental transitions in biparental rodents are limited, but the timing and length of these stages may vary among species. For example, while researchers typically wean prairie voles, mandarin voles, and Octodon degus at PND 21 (Keane et al., 2007, Wu et al., 2013, Uekita et al., 2019, Donovan et al., 2022), California mice are weaned between PND 30–35 (Bambico et al., 2015, Glasper et al., 2018, Agarwal et al., 2020, Walker et al., 2023, Wright et al., 2023), suggesting a later onset of the juvenile period. Additionally, California mice have a prolonged adolescent period, reaching adulthood at PND 90 (Wright et al., 2023), unlike uniparental rodents. It remains unknown if other biparental species share this extended adolescent period. Studying the effects of ELS on social behaviors across developmental stages may reveal to what extent early adversity disrupts social functioning and the development of brain regions involved in social behavior (see Fig. 2). This may help identify the timing and etiology of stress-related behaviors, guiding interventions to reduce long-term social impairments.

This review takes a novel approach to discuss sex differences in neuroplasticity following ELS. While many reviews have thoroughly addressed the interaction between sex and ELS, we postulate that the sex of the parent mediates the effects of ELS on neurobiological mechanisms associated with social behaviors. When reviewing findings from studies performed in animals, we focused on rodent studies utilizing prolonged maternal separation, maternal deprivation, LBN, and paternal deprivation paradigms. This review is not limited to rodent literature but also highlights relevant human research that examines the effects of parent–child relationships on neurobiological outcomes in the child. When referring to developmental stages (e.g., infancy, juvenile, adolescence) in humans and rodents, we use the age ranges provided in Fig. 1. Our review of the literature suggests that outcomes resulting from disruptions in interactions between offspring and the parent (i.e., ELS) are not consistent, and these outcomes may be related to the sex of the parent being manipulated.