Disruption of maternal parenting circuitry by addictive process: rewiring of reward and stress systems

Helena J V Rutherford, Sarah K Williams, Sheryl Moy, Linda C Mayes, Josephine M Johns, Helena J V Rutherford, Sarah K Williams, Sheryl Moy, Linda C Mayes, Josephine M Johns

Abstract

Addiction represents a complex interaction between the reward and stress neural circuits, with increasing drug use reflecting a shift from positive reinforcement to negative reinforcement mechanisms in sustaining drug dependence. Preclinical studies have indicated the involvement of regions within the extended amygdala as subserving this transition, especially under stressful conditions. In the addictive situation, the reward system serves to maintain habitual behaviors that are associated with the relief of negative affect, at the cost of attenuating the salience of other rewards. Therefore, addiction reflects the dysregulation between core reward systems, including the prefrontal cortex (PFC), ventral tegmental area (VTA), and nucleus accumbens (NAc), as well as the hypothalamic-pituitary-adrenal axis and extended amygdala of the stress system. Here, we consider the consequences of changes in neural function during or following addiction on parenting, an inherently rewarding process that may be disrupted by addiction. Specifically, we outline the preclinical and human studies that support the dysregulation of reward and stress systems by addiction and the contribution of these systems to parenting. Increasing evidence suggests an important role for the hypothalamus, PFC, VTA, and NAc in parenting, with these same regions being those dysregulated in addiction. Moreover, in addicted adults, we propose that parenting cues trigger stress reactivity rather than reward salience, and this may heighten negative affect states, eliciting both addictive behaviors and the potential for child neglect and abuse.

Keywords: addiction; human; parenting; preclinical; reward; stress.

Figures

Figure 1
Figure 1
The relationship between addiction and parenting. In our model, addiction represents the dysregulation of stress and reward systems, both of which are adapted to support parenting. In the addicted situation we propose that drug-induced brain changes result in the rewarding value of infant cues being attenuated, replaced by a more stressful neurophysiological response. This stress response to infant cues may increase craving for drugs of abuse, promoting drug seeking and relapse in abstinent mothers, and perpetuates the cycle of neglect.
Figure 2
Figure 2
The relationship between neurocircuits of stress, reward, and parenting. Parenting circuitry (red) shares many regions with stress (blue) and reward (yellow). The regions listed in the center have been implicated in all three circuits, suggesting that disruption in regions of one circuit can have profound impact on the functioning of the other connected circuits. It can be seen by the number of regions included in the Parental Circuitry circle that performance of optimal parental care (and the many types of behavior that fall into this category) requires typical functioning of the majority of the brain. Color coding in the legend indicates the anatomical brain systems in which each region belongs.
Figure 3
Figure 3
Oxytocinergic projection in the rodent brain. Oxytocin release is anatomically suited to signal in reward, stress, and maternal circuitries. The magnocellular neurons of the PVN (red oval) and SON (blue oval) project to the posterior pituitary to release OT peripherally in response to suckling or stressful stimuli. The parvocellular neurons of the PVN also project to the reward circuitry (VTA and NAc), stress circuitry (hippocampus, AMY, and intra-PVN release), and maternal circuitry (MPOA/BNST and OB), and are believed to be critical for appropriate social interactions. PVN, paraventricular nucleus of hypothalamus; SON, supraoptic nucleus of hypothalamus; VTA, ventral tegmental area; NAc, nucleus accumbens; AMY, amygdala; MPOA, medial preoptic area of the hypothalamus; OB, olfactory bulb. Brain schematic adapted from Paxinos and Watson (1997).
Figure 4
Figure 4
Reward circuitry in the rodent brain. This midline sagittal slice of rodent brain depicts the main brain regions implicated in responding to rewarding stimuli. The ventral tegmental area (VTA) of the midbrain sends dopaminergic projections (blue arrows) to the nucleus accumbens (NAc) and medial prefrontal cortex (mPFC). The NAc (as well as the lateral habenula, LHb) send GABAergic projections (red arrows) to the VTA, while the mPFC sends glutamatergic projections (green arrows) to the VTA. The mPFC and NAc have reciprocal glutamatergic projections. Activity changes in the NAc results in reward seeking or incentive behaviors (black arrow). Brain schematic adapted from Paxinos and Watson (1997).
Figure 5
Figure 5
Stress circuitry in the rodent brain. The paraventricular nucleus (PVN) in the hypothalamus sends corticotrophin releasing factor (CRF) projections (green arrows) to the central amygdala (CeA), bed nucleus of the stria terminalis (BNST), and the pituitary gland. The pituitary gland releases adrenocorticotrophic hormone (ACTH) into the blood stream that travels to the adrenal gland. Adrenal gland releases corticosterone (CORT) into the bloodstream. CORT acts as a negative feedback signal (red arrows) on the pituitary, PVN, and hippocampus, which sends excitatory projections to the PVN (green line arrows). The PVN receives additional excitatory input from the CeA and BNST. Brain schematic adapted from Paxinos and Watson (1997).
Figure 6
Figure 6
Role of brain changes in the relationship between drug use and parenting. Drug use is known to cause a number of brain changes (teal boxes and arrows). These changes can influence each other (red double-tipped arrows) by either amplifying or diminishing alterations depending on the behavioral and biological context. Importantly, these changes have independently been shown to contribute to parental care behaviors and when disrupted by drug use, results in reduced sensitivity to the rewarding value of infants and heightened stress. The stress response may be sufficient to trigger drug craving leading to continued drug use and relapse in abstinent mothers. In addition, drug seeking to reduce stress may also perpetuate the cycle of neglect.

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