SUD is characterized by a set of psychological and behavioral features which likely result from the development of tolerance, psychological and physiological dependence, and addiction. The persistence of addiction is due to mechanisms of reinforcement that can be both positive and negative. For example, positive reinforcement is the reward response that follows first consumption; a pleasurable experience with the drug leads to increased likelihood of further consumption. Conversely, the protracted use of the substance to avoid or soothe aversive withdrawal symptoms is considered a negative reinforcement that prolongs drug-intake behaviors and makes extinction more difficult (11). At a neurobiological level, reinforcement and relaps are modulated by both reward circuits and the stress response system (12). It is noteworthy that neurobiological changes occur in mothers' brains during the first few months after birth, mainly in brain regions designated to regulatory circuits, emotional responses, reward processing, executive functions, and parental behaviors (10). Processes implicated in drug addiction and mothering overlap at the neurobiological and psychological levels. Merging these considerations in the context of drug-abusing mothers renders it necessary to examine overall parent-infant interaction from a relational systems perspective that includes physiological and psychological needs of the mother, within a bioecological framework, so as to explicate the significance of autonomic mechanisms (13). Applying a physio-bioecological approach to the specific case of parenting in mothers with substance use disorders, the main aims are to uncover the effects that illicit drugs exert on maternal practices and parental styles in the domain of early mother-infant interaction, and to identify differences in maternal responses to infant stimuli between clinical and non-clinical populations.

Affiliative behaviors fall within the purview of the dopamine and oxytocin reward systems, which overlap with neural structures and pathways related to drug abuse and parental behavior. Hence, in mothers with issues pertaining to drug consumption, activation of one circuit may occur at the expense of the other. More concretely, the reward system could be involved in drug-seeking behaviors, with negative implications for mothering behaviors. Furthermore, brain areas related to perception and elaboration of infant cues, such as the prefrontal cortex, might be engaged in overcoming actions related to drug consumption, leading to subsequent higher levels of stress, thus affecting interactions with the infant (14).

In the case of cocaine-exposed mothers, neurohormonal pathways (especially those regulating oxytocin) can be altered, leading to decreased neurohormonal levels that affect neural responses to infant cues (15). Illicit substances impact motivation circuits implicated in parenting regulation (16) and maternal practices, such as infant feeding. In cocaine-abusing women, evidence points to a tendency for poor infant engagement (11) which deteriorates over the course of the first year of postnatal life (17); these effects are accompanied by shorter duration feeding sessions and diminished cognitive flexibility (18). Even among those receiving treatment, women exposed to opioids bear infants with neonatal abstinence syndrome and are less keen to breastfeed (19). Breastfeeding, while under opioid-treatment or not, has both short- and long-term consequences on dyadic attachment (20). SUD alters neurotransmission in the nucleus accumbens (NAcc), the prefrontal cortex (PFC), and ventral tegmental area (VTA). Functions in these areas become disrupted, with changes occurring in systems that regulate neurotransmitter levels in the forebrain and midbrain, like the transmission of serotonin and dopamine in the NAcc, and dysregulation of the hypothalamic-pituitary-adrenal axis (HPA) (12). These pathways enhance substance use relapse and augment negative affect, especially in women (4). Oxytocin modulates addiction-related behaviors, such as acquisition, withdrawal, drug-seeking, and relapse (15). Oxytocin contributes to social affiliative parenting behaviors. Not only is it involved in regulating uterine contractions during labor and milk ejection in breastfeeding, it is also pertinent to mother-infant bond formation and parental practices, eventually shaping the infant's own oxytocin profile (21). Although dopamine and oxytocin are different neurotransmitters, their pathways appear to be interlaced and, to a certain extent, overlap; thus, disruption of these systems can impact a multiplicity of mechanisms and behaviors related to both parenting and substance use (22). Indeed, during the early stages of development, infants express their needs through cries and facial expressions, and maternal drug consumption can alter maternal perceptions of these signals (23). For instance, modifications in perception of infant cues may manifest through a delay in facial recognition ERP responses to cry (24), and a reduction in activation of dopamine- and oxytocin-innervated brain regions while looking at their own baby's face (25, 26).

Drug addiction and motherhood are both accompanied by specific cerebral morphological and neurophysiological changes. Functional Magnetic Resonance Imaging (fMRI) studies on postpartum mothers' brains show an increase in gray matter volume in morphological structures, such as the hypothalamus, striatum, amygdala, thalamus, and insula, which are associated with the reward circuit, motivation, sensory information processing, emotional regulation, and empathy (26, 27). In an fMRI study, Landi and colleagues (14) compared neurophysiological activation patterns in response to infant stimuli between cocaine-exposed and non-exposed mothers. The clinical sample showed reduced neural activation in prefrontal areas, occipital lobes, and limbic structures (amygdala and parahippocampus) while looking at infant faces. The authors also reported decreased neural activation in the insula and auditory sensory areas while drug-abusing women were listening to infant cries (14). Prolonged diminished neural responses in these regions might compromise maternal behavior toward infants' needs and cues, with negative implications on mother-infant attachment (28).

Motherhood comes with a series of neurobiological modifications, representing a vulnerable temporal window for the development of depressive symptoms and changes in psychological states. We have reported studies highlighting the involvement of the reward circuit and amygdala in mechanisms motivating maternal behaviors (26, 27). These two areas are functionally connected to prefrontal cortical regions during emotion regulation through the use of cognitive strategies, such as reappraisal (29). The same substrates are implicated in drug consumption pathways that impair executive function, a multidimensional construct that includes, besides emotion regulation, a suite of cognitive operations like mental flexibility, inhibition, planning, working memory, reflective functioning (30), verbal fluency (31), and language (22, 32).

Struggles with emotion regulation in substance-abusing mothers might reinforce drug usage as a strategy to deal with stress, instead of developing or enhancing more adaptive regulatory skills, thus further aggravating emotional dysregulation (32). Difficulties in emotional regulation make it more challenging for drug-abusing mothers to maintain correct perceptions of their child's affective needs. At the same time, altered mechanisms of the reward circuit have implications for maternal parenting practices: for instance, the reward system might be more responsive to substance abuse, leading to maladaptive mother-infant interaction characterized by emotional disengagement and less responsive behaviors (24, 33, 34), (14, 35). Furthermore (16), quality of parenting might vary in a dose-dependent manner according to the quantity of drug consumed (17, 36). As a consequence, the demands for care which stand at the core of the mother-infant relationship may turn into a struggle, and fail to offer sufficient reward to addicted mothers, who are likely to adopt avoidant behaviors (11, 37) (see Figure 2).

Mother-infant attachment has become one of the most important concepts in developmental and clinical science since Bowlby published “Attachment and Loss” (38). Applying principles of attachment theory to the frame of substance-using mothers, individual characteristics of mother and infant alike define the nature of their interactions, so it is important to elucidate how specific drugs might alter mother-infant communication (39). Cocaine consumption during pregnancy compromises the quality of mother-infant interactions by altering maternal behaviors, such as warmth (40) and harshness (41), and infants of cocaine-abusing mothers are less responsive during play interactions (20, 24). Prenatally cocaine-exposed children undergo neurobehavioral changes, such as irritability, hypersensitivity, and difficulties in regulating emotional state that appear to prevent them from responding functionally to maternal stimuli; they may also appear lethargic, using sleepiness as a strategy to withdraw from stressful stimulation (42). Postnatal cocaine use has been reported to predict maternal insensitivity during interactions 8 weeks after birth (43). Overall, the quality of cocaine-mother and infant interaction is hallmarked by reduced mutual enjoyment, reciprocity, and regulation (33). However, some results in literature report that maternal cocaine use does not affect social interaction and attachment patterns at 12 (44) or 18 months (45). In general, an appropriate dyadic interaction requires high maternal sensitivity to infant cues. In this context, the concept of sensitivity implies the capacity to detect and accurately understand the child's signals and to respond appropriately according to the child's needs. This skill requires reflective abilities, such as mentalization, which appears to be impaired in drug-abusing mothers with regard to meeting the baby's needs and their own parental competencies (31). Frequently, mothers with low mentalizing capabilities attributable to substance use misunderstand infant behaviors, interpreting them as rejecting, and hence construct a representation of their child as intrusive, detached, or hostile (31, 42). Abuse of drugs during motherhood may result in “blue moods,” feelings of guilt, and inadequacy, which prevent the mother from being emotionally available in interactions with her offspring (42). Studies of drug-abusing mothers with more than one child have highlighted mothers' strain in delivering educational practices to older children, which point to difficulties in adjusting parenting behaviors that accord with developing requirements in their children (46).

Drug abuse is related to the context of social relationships (especially when it develops into an addiction) due to its implications for users and for related people, such as families, other addicts, partners, and, of course, children (47). Substance-abusing mothers display more problematic behaviors during interactions and experience less social support and greater environmental difficulties, like domestic violence and other forms of abuse (48, 49). Socially rewarding experiences and relationships are protective factors against drug-seeking behaviors (50). Conversely, dysfunctional relationships can prompt drug abuse or relapse, especially during the perinatal and postpartum periods. During this time frame, there is a higher probability that women will become victims of intimate partner violence (IPV) (51), which is defined as the experience of “physical violence, sexual violence, stalking and psychological aggression, including coercive acts, by a current or former intimate partner” (52). When occurring during pregnancy, IPV has been correlated with adverse gestational events, such as preterm delivery and low weight at birth (53). Together with pregnancy intentions (e.g., unintended), IPV during the postpartum period is associated with increased use of substances in women as a mechanism to cope with stress (54, 55). Mothers who experience IPV often show hyper-controlling, overly permissive, or unresponsive maternal behaviors, along with poor emotional sustenance, leading to negative child developmental outcomes (51, 56). Mogro and colleagues reported that, contextually, a scarce social network can increase the risk of exposure and perpetration of IPV (57). Excepting some interventions, there is a notable gap in the literature about social support provided to drug-abusing mothers based on their social network; such support could represent a source of positive emotional help. Women with substance use issues have been reported to belong to limited social networks, providing them inadequate social support (58). Other contextual circumstances likely affect maternal behavior, such as the risk of losing custody of the child, which is twice as likely in substance-using compared to non-using mothers (59).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.