Parenting and Addiction: Neurobiological Insights

Abstract

Addiction remains a significant public health concern that affects multiple generations within families, and in particular the early relationship between parents and their developing child. This article will discuss recent advances in our understanding of the neurobiology of parenting and addiction. Specifically, the discussion will focus on the reward-stress dysregulation model of addicted parenting, which proposes that the dysregulation of stress and reward neural circuits by addiction represents a neurobiological pathway through which to understand how caregiving may be compromised in addicted parents. Empirical research in parents and non-parents will be discussed in support of this model and critical consideration of the model and its limitations will be provided.

Introduction

Addiction remains a significant concern for women and their developing child during pregnancy and the postpartum period, despite numerous prevention and intervention efforts [1]. While a vast literature exists on behavioral correlates of human parenting and addiction, a contemporary approach has adopted a neurobiological perspective to understanding how caregiving may be disrupted by addiction. The advantage of this neurobiological approach is the opportunity to probe neural circuitry critical to parenting that may be compromised by addiction, and identify mechanisms through which neurochemical effects of substance abuse may exert an influence on caregiving. This article will review one of the current neurobiological models of addicted parenting, the supporting evidence, and a critical consideration of its advancement.

Parenting and Addiction: A Reward-Stress Dysregulation Model

Addiction has been conceptualized as disorder of dysregulation in the neural circuits of reward and stress reactivity and regulation, underscored by a transition from positive to negative reinforcement mechanisms [2,3]. Specifically, initial substance use is maintained by the hedonic properties of the drug (i.e., positive reinforcement), consistent with findings that most substances of abuse activate reward neural circuits innervated by dopamine [4]. Over time, activation of these same reward circuits weakens in response to the substance, and instead cues associated with substance use drive reward-based neural activity. Consequently, in addicted adults, the conditioned cue motivates drug-seeking behavior rather than the hedonic ‘high’ upon consumption [5]. Concurrent alterations to the stress neurocircuitry have been noted in addiction. Namely that the substance provides relief from negative affective states of craving and withdrawal, which reinforces continued and habitual substance use over time (i.e., negative reinforcement) [2,3]. This reliance on substances to provide relief may generalize to other negative emotional states, including stress, anxiety, and depression.

As highlighted in Figure 1, brain regions affected by addiction and associated with reward, including prefrontal cortex, ventral tegmental area, and nucleus accumbens (NAcc), and regions associated with stress, including the hypothalamic-pituitary-adrenal axis and extended amygdala, are also engaged when parents perceive infant stimuli and/or interact with infants [6]. Consequently, impairments observed in parenting may be secondary to the dysregulation of stress and reward neural circuits in addiction, which enables the identification of neurobiological pathways through which addiction impacts caregiving. The reward-stress dysregulation model of addicted parenting proposes that given aberrant reward-stress neural circuits, parenting and caring for a child is less rewarding and more stressful [6,7]. In the next sections, consideration will be given to each component of this model of addicted parenting.

Figure 1.

Overlapping neural circuits of stress (blue), reward (yellow), and parenting (red), with brain regions listed in the center of the diagram implicated in all three systems. The brain systems that brain regions belong to are illustrated by color coding in the legend. Figure as originally published in Rutherford HJV, Williams SK, Moy S, Mayes LC, and Johns JM (2011). Disruption of maternal parenting circuitry by addictive process: rewiring of reward and stress systems. Frontiers in Psychiatry 2:37. http://dx.doi.org/10.3389/fpsyt.2011.00037

Decreased Salience of Infant Signals

Infants and caregiving are inherently rewarding. Even in non-parents, perception of infant faces activates the NAcc [8], and in parents, infant faces reliably elicit activity in reward neural circuits [6,7]. These studies suggest the inherent properties of infant faces are rewarding and may attract the attention of, and promote behavior from, potential caregivers [9]. One component of the reward-stress dysregulation model of addicted parenting suggests that the co-optation of reward neural circuitry by addiction compromises the salience of other rewards, including socio-affiliative relationships (c.f., [10]). Therefore, infant cues may be less rewarding and less salient to addicted parents, perhaps explaining the withdrawn, passive, and disengaged caregiving that has been observed in dyadic interactions [11,12] (Figure 2). Empirical research has reported a decreased neural response to monetary reward cues in the ventral striatum (which includes the NAcc) of addicted non-parents [13,14]. Further, non-treatment-seeking cocaine-dependent participants, relative to controls, evidenced decreased neural responding to emotional stimuli, an effect pronounced in female participants [15]. Such findings converge with the hypothesis that addiction may compromise neural circuits implicated in reward and affective processes even before the transition to parenthood.

Figure 2.

In response to an infant signal, a cascade of processes may underscore maladaptive parenting determined by aberrant reward (in yellow) and stress (in blue) neural circuits.

Only a handful of studies have examined the impact of substance abuse on the neural circuits of human parenting. One functional magnetic resonance imaging (MRI) study reported that substance-using mothers, relative to non-substance-using mothers, evidenced a decreased response to infant cues (faces, cries) in sensory processing, prefrontal, and limbic regions (including the amygdala and parahippocampus) [16]. A second event-related potential study reported that maternal tobacco-smokers had a delayed neural response to infant faces, as compared to non-smoking mothers [17]. This hypo-reactive response to infant stimuli in substance-using mothers supports the hypothesized decreased salience of these infant affective cues consistent with the reward-stress dysregulation model. These neuroimaging findings also resonate with behavioral studies of observed dyadic interactions where mothers with substance use disorders are more passive and disengaged [11,12]. Mechanistically, decreased salience of infant affective cues may diminish perceptual and attentional processing and therefore subsequent responding during behavioral encounters between parents and their children [18]. Of note, multiple therapeutic approaches have been designed to enhance mothers’ internal representation of their child, and in doing so increasing the rewarding of caregiving, the salience of their infant, and improving dyadic outcomes [19].

Increased Stress of Caregiving

While inherently rewarding, parenthood also encapsulates periods of stress, which may begin prenatally and continue across the lifespan impacting the familial system [1]. Substance use has been well associated with stress-related symptomatology [20] and exposure to stress increases subjective reports of craving that correlate with activity in brain regions such as the dorsal striatum and caudate [21]. Activation in neural circuits during stress inductions appear to overlap with activation in neural circuits during cue-induced drug craving inductions [22], suggesting a common pathway through which these two systems interact. Consistent with negative reinforcement models of addiction [2,3], addicted individuals may rely on substance use to alleviate negative affective states, including stress. The reward-stress dysregulation model of addicted parenting hypothesizes that stress responses to infant affective cues may lead to increased craving for substance use that through past experience has been associated with relief of negative affect states. This may be particularly true early postpartum as a critical period of vulnerability given the demands of caring for an infant. Therefore, parents may relapse postpartum if they were able to abstain during the pregnancy or else continue to use substances during the postpartum period (Figure 2). Evidence is beginning to emerge in support of this notion. Tobacco-smoking mothers who relapsed postpartum report higher stress, depression, and anxiety scores than mothers who did not relapse following abstinence during their pregnancy [23]. Furthermore, episodes of infant crying and irritability have been associated with triggers of substance-using cognitions and behaviors [24].

There are clear clinical implications to support parents in facilitating their emotional responses postpartum given the dysregulation of the stress system in addiction. Indeed, understanding how parenting-related stress may be a critical mechanism for relapse informs intervention approaches for parents to specifically focus on the stressors of their caregiving role. Relatedly, therapeutic work with mothers in methadone-maintenance has identified compromised parental reflective functioning in this maternal group [26], which refers to a cognitive capacity to understand the thoughts, feelings, and emotions of the infant, and this capacity may also be diminished by stress [27]. Higher levels of reflective functioning have been associated with behavioral measures of maternal tolerance of [28], and neural markers of heightened attention allocation towards [29], infant cries. Given the closely coupled relation between stress and addiction, and the breadth of parenting functions likely impacted by stress, including reflective functioning, probing stress neurocircuitry in addicted parents is of critical importance.

Advancing the Reward-Stress Dysregulation Model

Adopting a neurobiological perspective to addicted parenting has proved valuable in beginning to identify mechanisms that underscore the disrupted caregiving behaviors associated with addiction. This approach has afforded a clear pathway to measuring the interplay between reward and stress neural circuits in contributing to caregiving behavior in parents with substance use disorders. However, significant progress is needed to broaden the scope of this model.

In the empirical studies to date, the neurobiology of addicted parenting has been examined in response to the presentation of infant affective cues as experimental stimuli in maternal samples. However, it will be important to examine these same studies in fathers, and advance neurobiological investigations by addressing functional and structural brain activity in addicted parents even before the presence of infant emotional signals. One structural MRI study [30] reported that substance-using mothers had an overall reduction in gray matter (GM) volume of the brain, particularly in frontal brain regions. In bridging brain to behavior in this latter study, substance-using mothers with greater GM reductions reported higher levels of behavioral activation – a motivational construct implicated in impulsivity. Another study employed electroencephalography, and reported differential patterns of neural oscillations at rest between tobacco-smoking and non-smoking mothers [31]. Together these studies suggest there may be value to interrogating the neural circuitry of parenting even before responses to infant affective cues are assessed.

An important advance of this work must incorporate the recognition that addiction typically presents in patients managing a host of socioeconomic, interpersonal, and psychiatric challenges. Therefore, the extent to which brain and behavioral correlates of addicted parenting truly reflect substance abuse and dependence or the myriad of factors that are associated with addiction requires further investigation. This approach would encompass understanding how other relevant variables important to parenting are affected by addiction (e.g., reflective functioning). Our understanding of parenting and addiction may be limited by cross-sectional studies at the onset of parenthood. Addiction may be better conceptualized as a developmental disorder, wherein early adverse experiences may shape neurocognitive functioning across development and increase vulnerability to substance use in adolescence and adulthood, and suboptimal caregiving with the onset of parenthood [32] (Figure 3). This re-conceptualization would identify pathways through which intergenerational transmission of compromised caregiving may be further understood. A number of neurocognitive systems have been implicated in this trajectory to substance use, including modifications to reward processes and executive functioning [33]. Oxytocin, dopamine, and glutocorticoid systems have also been identified as important in developmental pathways to addiction following early adversity [34]. Consequently, empirical approaches to parenting and addiction would benefit greatly from a developmental lens to more sensitively tease apart pathways to compromised parenting in substance abusing and addicted parents.

Figure 3.

A developmental lens of the potential pathways to addiction and how this may compromise subsequent caregiving behavior. The timeline illustrates periods of vulnerability to early adversity and substance use as well as other risk factors that may increase initiation and maintenance of substance use.

The reward-stress dysregulation model presented here provides a broad and overarching framework to consider the interplay of reward-stress neural circuits in addicted parenting. However, greater specificity regarding mechanisms of reward and stress are required. For instance, emerging research in preclinical studies suggests that reward can be dissociated into different components of “wanting”, “liking”, and “learning” [35,36]. Of relevance to the reward-stress dysregulation model is the distinction between “wanting” and “liking”. Reward wanting reflects the motivational component of reward that drives behavior toward or away from a stimulus. Reward liking encompasses the hedonic or pleasurable component in the receipt of reward. For some mothers, the “wanting” to care for their infant could be preserved but their pleasure or enjoyment in caregiving (i.e., “liking”) is compromised. Similarly, mothers may “like” interactions with their infant, but caregiving motivation (i.e., “wanting”) may be attenuated, and the drive or approach toward their infant is absent. In non-depressed mothers listening to infant cries, increased neural activity in reward brain regions was observed, presumably promoting approach motivation toward the infant (i.e., “wanting”). This effect was attenuated in depressed mothers [37]. Therefore, a more nuanced understanding of reward processes may inform where to target intervention most effectively, providing objective indicators of underlying neurobiological mechanisms that compromise parenting.

Conclusions

The reward-stress dysregulation model proposes that the dysregulation of reward-stress neural circuits by addiction presents a neurobiological pathway through which to understand how caregiving may be compromised in addicted parents. Clear mechanisms can be identified and measured, with preliminary neuroimaging data confirming the decreased salience of infant cues to substance-using mothers. More evidence is needed, including a greater focus on stress reactivity and regulation, as well as research providing a developmental lens through which to understand how early experiences shape the trajectory to addiction and impacts parenting. Such evidence necessitates an interdisciplinary approach, including the study of parents and non-parents, in the presence and absence of addiction, to afford the opportunity for exploration of causal pathways and the potential reversibility of addiction effects on parenting. Nevertheless the reward-stress dysregulation model provides an important basis for hypothesis generation and theoretical refinement as this research continues.

Highlights.

• Addiction impacts caregiving behavior

• Reward and stress neural circuits are dysregulated in addiction

• Parenting brain regions overlap with dysregulated reward-stress systems

• A neurobiological approach is adopted to investigate addicted parenting