Pathways Relating the Neurobiology of Attachment to Drug Addiction

Lane Strathearn, Carol E Mertens, Linda Mayes, Helena Rutherford, Purva Rajhans, Guifeng Xu, Marc N Potenza, Sohye Kim, Lane Strathearn, Carol E Mertens, Linda Mayes, Helena Rutherford, Purva Rajhans, Guifeng Xu, Marc N Potenza, Sohye Kim

Abstract

Substance use disorders constitute a significant public health problem in North America and worldwide. Specifically, substance addictions in women during pregnancy or in the postpartum period have adverse effects not only on the mother, but also on mother-infant attachment and the child's subsequent development. Additionally, there is growing evidence suggesting that parental addiction may be transmitted intergenerationally, where the child of parents with addiction problems is more likely to experience addiction as an adult. The current review takes a developmental perspective and draws from animal and human studies to examine how compromised early experience, including insecure attachment, early abuse/neglect, and unresolved trauma, may influence the development of neurobiological pathways associated with addictions, ultimately increasing one's susceptibility to addictions later in life. We approach this from three different levels: molecular, neuroendocrine and behavioral; and examine the oxytocin affiliation system, dopamine reward system, and glucocorticoid stress response system in this regard. Increased understanding of these underlying mechanisms may help identify key targets for early prevention efforts and inform needed intervention strategies related to both insecure attachment and addiction.

Keywords: addiction; adverse childhood experiences; attachment; dopamine; glucocorticoid; oxytocin.

Copyright © 2019 Strathearn, Mertens, Mayes, Rutherford, Rajhans, Xu, Potenza and Kim.

Figures

Figure 1
Figure 1
Developmental and neurobiological pathways linking adverse childhood experience to susceptibility to addiction, via modifications in dopamine-related, oxytocin-related, and glucocorticoid-related systems at molecular, neuroendocrine, and behavioral levels. Childhood adversity, including abuse and neglect, may be associated with insecure attachment, and lead to behavioral patterns linked with specific patterns of substance abuse. Parental addiction may impair parental caregiving capacity as a result of insecure patterns of adult attachment, and perpetuate the cycle of childhood adversity and addiction. DA, dopamine; OT, oxytocin; GC, glucocorticoid; rec, receptor; CRF, corticotropin-releasing factor; PFC, prefrontal cortex; HPA, hypothalamic–pituitary–adrenal; PTSD, post-traumatic stress disorder. Adapted from (3) © 2016 New York Academy of Sciences. Used with permission from John Wiley and Sons.
Figure 2
Figure 2
The neurobiology of attachment, incorporating 1) dopamine-related “reward/reinforcement” and “habit” pathways, 2) oxytocin-related “affiliation” pathways, and 3) glucocorticoid-related stress-response pathways. Secure patterns of attachment are associated with greater activation of the mesocorticolimbic and oxytocin-associated circuits, whereas insecure/dismissing attachment is associated with greater activation of nigrostriatal dopamine pathways. Adapted from (36) © 2011 The Author, Journal of Neuroendocrinology. © 2011 Blackwell Publishing Ltd. Used with permission from John Wiley and Sons.
Figure 3
Figure 3
Plasma oxytocin response to mother–infant interaction is reduced in mothers with insecure/dismissing attachment, compared with securely attached mothers (A), and is correlated with activation of hypothalamus (rs = 0.6, p = 0.001) and ventral striatum (rs = 0.57, p = 0.001), in response to viewing own-infant faces in a functional MRI scanner (B). (36) Adapted from (24) © 2011 The Author, Journal of Neuroendocrinology. © 2011 Blackwell Publishing Ltd. Used with permission from John Wiley and Sons.
Figure 4
Figure 4
Both major depressive disorder (MDD) and high-risk groups (with current depression in mother but not in adolescent) show attenuated right ventral striatum activation in response to a standard reward outcome during functional MRI scanning (both *p

Figure 5

(A) Mothers with no unresolved…

Figure 5

(A) Mothers with no unresolved trauma show a greater amygdala response to sad…
Figure 5
(A) Mothers with no unresolved trauma show a greater amygdala response to sad than happy infant faces (z = 3.00, p = 0.003), whereas (B) mothers with unresolved trauma show a blunted amygdala response to their own infant’s distress cues during functional MRI scanning (z = -2.38, p = 0.017). BOLD (blood-oxygen-level-dependent) signals were extracted from a bilateral amygdala mask (shown left) and submitted to mixed-effects linear regression analysis. Adapted from (138). Used with permission from Taylor & Francis Ltd.

Figure 6

In response to own- vs.…

Figure 6

In response to own- vs. unknown-infant happy faces (OH > UH), mothers with addiction…

Figure 6
In response to own- vs. unknown-infant happy faces (OH > UH), mothers with addiction problems show deactivation in the hypothalamus, ventral striatum, and ventromedial prefrontal cortex, regions wherein strong activation has been observed in mothers without a history of substance use (random effects analysis; FDR-corrected p < 0.05). Inset shows brain response time courses extracted from the peak voxels in each specified region (hashed line circle), after presentation of own-happy (green plot) and unknown-happy (red plot) infant face cues between 0 and 2 seconds. Adapted from (139). © 2017 Wiley Periodicals, Inc. Used with permission.
Figure 5
Figure 5
(A) Mothers with no unresolved trauma show a greater amygdala response to sad than happy infant faces (z = 3.00, p = 0.003), whereas (B) mothers with unresolved trauma show a blunted amygdala response to their own infant’s distress cues during functional MRI scanning (z = -2.38, p = 0.017). BOLD (blood-oxygen-level-dependent) signals were extracted from a bilateral amygdala mask (shown left) and submitted to mixed-effects linear regression analysis. Adapted from (138). Used with permission from Taylor & Francis Ltd.
Figure 6
Figure 6
In response to own- vs. unknown-infant happy faces (OH > UH), mothers with addiction problems show deactivation in the hypothalamus, ventral striatum, and ventromedial prefrontal cortex, regions wherein strong activation has been observed in mothers without a history of substance use (random effects analysis; FDR-corrected p < 0.05). Inset shows brain response time courses extracted from the peak voxels in each specified region (hashed line circle), after presentation of own-happy (green plot) and unknown-happy (red plot) infant face cues between 0 and 2 seconds. Adapted from (139). © 2017 Wiley Periodicals, Inc. Used with permission.

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