Maternal opioid use disorder and brain physiology during empathy

• In Event: Perinatal Substance Use affects the Neural Basis of Mother-Infant Attachment

Abstract

Background: The prevalence of pregnant women with opioid use disorder (OUD) in the U.S. quadrupled in the past 15 years. Gold standard treatment of buprenorphine medication (BM/OUD), to prevent withdrawal and miscarriage, still leaves 33%+ relapsing to substance use. BM/OUD mothers are at high risk of insensitive parental behaviors, known to be governed by an evolutionary conserved Maternal Behavior Neurocircuit (MBN) toward maternal caring and defensive/aggressive behaviors - normally under reciprocal regulation. The knowledge gap on the effects of BM/OUD on MBN adaptation in the early postpartum is magnified by the transgenerational risks for affected mother-infant dyads. For this longitudinal magnetic resonance imaging (MRI) study, we hypothesize that the MBN adapts in early postpartum as a function of BM/OUD, mood, and parenting stress.

Methods: We studied 79 mothers in early PP, 42 of which completed brain imaging at two time-points: T1 (1 month PP) and T2 (4 months PP). Participants reported depression symptoms and stress using Beck Depression Inventory and parenting stress index respectively at T1 & T2. We divided the participants into three groups: BM/OUD (n=11), non-opioid depressed control (DC, n=12), and non-opioid non-depressed healthy controls (HC, n=19). At each timepoint, the participants underwent functional magnetic resonance imaging (fMRI) scans while performing 3 tasks: a baby-cry task, wherein subjects listened to own and other's baby cry and respective control sounds in a block design (30s per block, 5 blocks per condition); a baby-face mirroring task, wherein subjects were asked to join (empathic mirroring) or observe (unresponsively observing) own or unknown child’s face pictures of neutral, ambiguous, distressful, and joyful expressions - in a block design of four consecutive pictures (4s/picture, one picture per emotional expression); and a resting state task of 8 minutes. fMRI data were processed and analyzed in SPM 8.

Results: While BM/OUD mothers showed comorbid depressive mood symptoms like DC mothers, they exhibited higher child-oriented worries than DC/HC mothers. Own vs. other's baby cry responses and relative brain volumes in the MBN show BM/OUD>DC/HC brain physiology correlating with maternal worries. However, resting-state functional connectivity (rs-FC) between MCN neurocircuits that mediate caregiving vs. defensive behaviors in animal models, was not antagonistic for BM/OUD mothers as among DC/HC mothers. The Child Face Task identified the dorsomedial prefrontal cortex as differentially deactivated for emotional attunement to child’s feelings as opposed to distantly observing (Join vs Observe, Own vs. Other Child).

Conclusions: During the early postpartum, BM/OUD influences the early postpartum, adaptation of maternal brain and behaviors. BM/OUD appears to increase maternal behavior neurocircuit (MCN) responses and rs-FC in caregiving MCN. However, BM/OUD also increases defensive MCN activity and interferes with normal rs-FC between caregiving and defense neurocircuits. Furthermore, evidence from the child face task suggests that the dmPFC may be hijacked by addiction – potentially dysregulating the MBN and leading to exacerbated parenting stress. Thus, BM treatment appears may drive maternal brain physiology toward maternal behavior, consistent with the benefits of treatment – yet may also pose risks for exacerbated postpartum stress and reduced maternal sensitivity.

Authors

• James E. Swain, Stony Brook Unviersity
  Presenting Author

• Shaun Ho, Stony Brook University
  Non-Presenting Author