Drug addicted mothers show reduced brain reward response to their infants: Can oxytocin reverse the trend?
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1 Drug addicted mothers show reduced brain reward response to their infants: Can oxytocin reverse the trend? Dr. Lane Strathearn, MBBS FRACP PhD Stead Family Professor, Department of, University of Iowa Director, Division of Developmental and Behavioral, and the Center for Disabilities and Development, University of Iowa Children s Hospital
2 Maternal care and addiction In 2011, 22.5 million (age 12+), 8.7% of the population, used illicit drug in the past month. Drug use is the highest among people in late teens and twenties. Almost 90% of drug-abusing women are of reproductive Maternal addiction is associated with a range of parenting difficulties, including child abuse and neglect US Department of Health and Human Services, 2012 Page 2 11/18/15 2:49:14 PM
3 Neglect/emotional abuse predicts teenage alcohol use Mills, 2013 Page 3 11/18/15 2:49:14 PM
4 Neglect/emotional abuse predicts teenage alcohol use Mills, 2013 Page 4 11/18/15 2:49:14 PM
5 Neglect/emotional abuse predicts teenage smoking Mills, 2013 Page 5 11/18/15 2:49:14 PM
6 Neglect/emotional abuse predicts teenage smoking Mills, 2013 Page 6 11/18/15 2:49:14 PM
7 Adverse Childhood Experience (ACE) Study Over adults retrospectively report adverse childhood experiences, such as: - abuse - neglect - witnessing domestic violence, and - serious household dysfunction An ACE score, based on the number of adverse conditions experienced in childhood, was linked to current and past medical and psychiatric conditions Page 7 11/18/15 2:49:15 PM
8 Adverse Childhood Experience (ACE) Study ACE score was progressively associated with an increased risk of: - coronary artery disease - chronic pulmonary disease - cancer - severe obesity - alcoholism - depression and anxiety - drug addiction - sexual promiscuity - perpetrating intimate partner violence Page 8 11/18/15 2:49:15 PM
9 ACE Score predicts substance use risk 11 Adjusted Odds Ratio ACE Score >=4 1 Alcoholic Illicit drug use Injected drugs Felitti, 1998 Page 9 11/18/15 2:49:15 PM
10 CHILDHOOD NEGLECT ADVERSE CHILDHOOD EXPERIENCE ABUSE AND TRAUMA? Increased susceptibility to addiction Impaired maternal brain response and caregiving behavior Page 10 11/18/15 2:49:15 PM
11 Possible Mechanisms 1. Cumulative exposures to stressful experiences 2. Latent effects of adversity during sensitive periods of development What are the molecular and neuroendocrine mechanisms underlying these differences in health and behavioral outcomes? Shonkoff et al, JAMA (2009) Page 11 11/18/15 2:49:15 PM
12 Maternal Behavior in the Rat Pup vocalization Licking and grooming Arched-back nursing Champagne, 2003 Page 12 11/18/15 2:49:15 PM
13 Frequency Distribution of Time Spent Licking/ Grooming by Lactating Mothers LOW MID HIGH % Licking & Grooming Champagne, 2003 Page 13 11/18/15 2:49:16 PM
14 National Institutes of Health Page 14 11/18/15 2:49:16 PM
15 Epigenetic regulation of infant development Two Examples 1. Stress Reactivity 2. Maternal Caregiving / Social Behavior Page 15 11/18/15 2:49:16 PM
16 Epigenetic regulation of infant development Stress Reactivity Offspring of High Licking/Grooming Rat Dams Ø ê DNA methylation of glucocorticoid (stress hormone) receptor (GR) promoter Ø é GR gene expression in the hippocampus Ø é regulation of stress response (glucocorticoid release) Ø ê stress/anxiety related behaviors Weaver et al, Nature Neuroscience (2004) Page 16 11/18/15 2:49:16 PM
17 Epigenetic regulation of infant development Caregiving behavior Offspring of High Licking/Grooming Rat Dams Ø ê DNA methylation of estrogen receptor-α (ERα) promoter Ø é ERα gene expression in the brain (MPOA) Ø é oxytocin receptor binding in the MPOA Ø é maternal caregiving/social behaviors (licking/grooming, arched back nursing) Champagne et al, Endocrinology (2006) Page 17 11/18/15 2:49:16 PM
18 RDoC categories Positive Valence Systems Approach motivation & reward valuation Social Processes Affiliation, attachment & social communication Negative Valence Systems Loss or threat (stress) Dopamine (DA) System Oxytocin (OT) System Glucocorticoid (GC) System CHILDHOOD NEGLECT ADVERSE CHILDHOOD EXPERIENCE ABUSE AND TRAUMA Genes/ Molecules/ Cells Circuits/ Physiology? Behavior/ Self-reports Increased susceptibility to addiction Page 18 11/18/15 2:49:16 PM
19 RDoC categories Positive Valence Systems Approach motivation & reward valuation Social Processes Affiliation, attachment & social communication Negative Valence Systems Loss or threat (stress) Dopamine (DA) System Oxytocin (OT) System Glucocorticoid (GC) System CHILDHOOD NEGLECT ADVERSE CHILDHOOD EXPERIENCE ABUSE AND TRAUMA Genes/ Molecules/ Cells Altered DA rec expression and DA production Altered OT rec expression and OT production Altered GC rec expression and CRF production Circuits/ Physiology Altered brain reward sensitivity (e.g. striatum) Altered brain sensitivity to social cues (e.g. PFC) Altered amygdala activation and HPA stress response Behavior/ Self-reports Sensation- or noveltyseeking; risk-taking behavior Social impairment, isolation and insecure attachment Anxiety, depression and trauma symptoms Increased susceptibility to addiction Impaired maternal brain response and caregiving behavior Page 19 11/18/15 2:49:17 PM
20 ? SENSORY INPUT (e.g. child face/cry cues) MOTOR OUTPUT (e.g. caregiving behavior) Page 20 11/18/15 2:49:17 PM
21 SENSORY INPUT (e.g. child face/cry cues) MOTOR OUTPUT (e.g. caregiving behavior) Page 21 11/18/15 2:49:17 PM
22 FOREBRAIN Frontal Cortex SENSORY INPUT (e.g. child face/cry cues) LIMBIC BRAIN Striatum MOTOR OUTPUT (e.g. caregiving behavior) MIDBRAIN Meso/Nigro Page 22 11/18/15 2:49:17 PM
23 VENTROMEDIAL PREFRONTAL CORTEX DORSOLATERAL PREFRONTAL CORTEX SENSORY INPUT (e.g. child face/cry cues) VENTRAL STRIATUM + AMYGDALA DORSAL STRIATUM + MOTOR OUTPUT (e.g. caregiving behavior) +/- +/- HYPO- THALAMUS ENDOGENOUS OXYTOCIN VENTRAL TEGMENTAL AREA + SUBSTANTIA NIGRA Mesocorticolimbic Dopamine Pathway: Reward Nigrostriatal Dopamine Pathway: Habit Formation Page 23 11/18/15 2:49:17 PM
24 Page 24 11/18/15 2:49:18 PM
25 Visit 1: Pregnancy Visit 1: Pregnancy Visit 2: Videotaping Visit 3: Scanning Visit 4: Follow-Up 3 rd trimester 7 mths 10 mths 14 mths Study Timeline BIRTH 20 min 5 min 6 min 20 min Mother-infant separation 1 CARE-Index Mirror-based interaction Motherinfant separation 2 Data Collected AAI-DMM Demographics PDQ BDI PANAS (1) Demographics ATQ Infant face images Blood draws Oxytocin Cortisol Adrenaline Noradrenaline PANAS (2) IBQ PSI WTAR Breastfeeding duration Hours separated per week Bayley Scales of Infant Development Strange Situation Procedure ADULT ATTACHMENT Page 25 11/18/15 2:49:18 PM
26 Visit 2: Videotaping Visit 1: Pregnancy Visit 2: Videotaping Visit 3: Scanning Visit 4: Follow-Up 3 rd trimester 7 mths 10 mths 14 mths Study Timeline BIRTH 20 min 5 min 6 min 20 min Mother-infant separation 1 CARE-Index Mirror-based interaction Motherinfant separation 2 Data Collected AAI Demographics PDQ BDI PANAS (1) Demographics ATQ Infant face images Blood draws Oxytocin Cortisol Adrenaline Noradrenaline PANAS (2) IBQ PSI WTAR Breastfeeding duration Hours separated per week Bayley Scales of Infant Development Strange Situation Procedure ADULT ATTACHMENT Page 26 11/18/15 2:49:18 PM
27 Visit 3: Scanning Visit 1: Pregnancy Visit 2: Videotaping Visit 3: Scanning Visit 4: Follow-Up 3 rd trimester 7 mths 10 mths 14 mths Study Timeline BIRTH 20 min 5 min 6 min 20 min Mother-infant separation 1 CARE-Index Mirror-based interaction Motherinfant separation 2 Data Collected AAI-DMM Demographics PDQ BDI PANAS (1) Demographics ATQ Infant face images Blood draws Oxytocin Cortisol Adrenaline Noradrenaline PANAS (2) IBQ PSI WTAR Breastfeeding duration Hours separated per week Bayley Scales of Infant Development Strange Situation Procedure ADULT ATTACHMENT BRAIN / HORMONE /BEHAVIOR Page 27 11/18/15 2:49:18 PM
28 Visit 4: Follow-Up Visit 1: Pregnancy Visit 2: Videotaping Visit 3: Scanning Visit 4: Follow-Up 3 rd trimester 7 mths 10 mths 14 mths Study Timeline BIRTH 20 min 5 min 6 min 20 min Mother-infant separation 1 CARE-Index Mirror-based interaction Motherinfant separation 2 Data Collected AAI-DMM Demographics PDQ BDI PANAS (1) Demographics ATQ Infant face images Blood draws Oxytocin Cortisol Adrenaline Noradrenaline PANAS (2) IBQ PSI WTAR Breastfeeding duration Hours separated per week Bayley Scales of Infant Development Strange Situation Procedure ADULT ATTACHMENT BRAIN / HORMONE /BEHAVIOR INFANT ATTACHMENT Strathearn L, et al. (2009) Neuropsychopharmacology. Page 28 11/18/15 2:49:18 PM
29 Group Comparisons Comparison of 15 Type B and 15 Type A mothers No significant group differences: -Maternal SES, race, education or IQ - Self-reported parenting stress - Pre- or post-natal depression - Psychopathology risk - Mother or infant temperament - Infant development at 14 months - Breastfeeding duration Page 29 11/18/15 2:49:18 PM
30 Secure vs. Insecure/Dismissing TYPE B TYPE A Medial PFC Orbitofrontal cortex Ventral striatum Dorsolateral PFC Page 30 11/18/15 2:49:19 PM
31 Own Happy Faces: Secure vs. Insecure Bilateral Ventral Striatum VS % Signal Change (se=1.0, t=3.0, p=0.006) 0 y=11-1 Secure Insecure/Dismissing mpfc (se=0.4, t=3.1, p=0.005) Right Medial PFC x=-6 % Signal Change Secure Insecure/Dismissing Page 31 Strathearn et al. Neuropsychopharmacology (2009) 11/18/15 2:49:19 PM
32 Secure vs. Insecure/Dismissing TYPE B TYPE A Medial PFC Dorsolateral PFC Orbitofrontal cortex Ventral striatum Ventral striatum Dorsolateral PFC Anterior insula Page 32 11/18/15 2:49:19 PM
33 Own Sad Faces: Type B vs. Type A 1.4 R Ventral Striatum VS VS % Signal Change (se=0.4, t=3.1, p=0.005) -0.4 y=11 y= Secure Insecure/Dismissing R Insula Insula % Signal Change (se=1.0, t=3.0, p=0.006) y=17 x= Secure Insecure/Dismissing Strathearn et al. Neuropsychopharmacology (2009) Page 33 11/18/15 2:49:19 PM
34 OXYTOCIN REGION A Serum Oxytocin (pg/ml) * Secure Insecure Strathearn et al. Neuropsychopharmacology (2009) DOPAMINE REGION B Brain Activation (beta weights) Hypothalamus Secure Insecure Brain Activation (beta weights) Ventral striatum Change in Oxytocin (%) Page 34 11/18/15 2:49:19 PM Change in Oxytocin (%)
35 Unresolved trauma in mothers Includes occurrences of childhood abuse, neglect, or death of a parent Current discourse from Adult Attachment Interview indicates that the trauma has not been adequately processed, and continues to interfere with current functioning In our cohort of mothers with addiction (n=44), 98% had unresolved trauma, vs. 67% of control mothers (n=18) (χ2=12.3, p<0.001). Page 35 11/18/15 2:49:19 PM
36 Amygdala activation to infant distress in mothers with unresolved trauma R 0.5 y = Amygdala Amygdala BOLD Signal Change (Estimated Marginal Means) A. No trauma Happy Sad ** B. Unresolved trauma Happy Infant Affect Sad Infant Identity Own Unknown Kim et al. Social Neuroscience (2014) Page 36 11/18/15 2:49:20 PM
37 What happens in addiction? VENTROMEDIAL PREFRONTAL CORTEX DORSOLATERAL PREFRONTAL CORTEX SENSORY INPUT (e.g. child face/cry cues) VENTRAL STRIATUM + AMYGDALA DORSAL STRIATUM + MOTOR OUTPUT (e.g. caregiving behavior) +/- +/- HYPO- THALAMUS ENDOGENOUS OXYTOCIN VENTRAL TEGMENTAL AREA + SUBSTANTIA NIGRA Mesocorticolimbic Dopamine Pathway: Reward Nigrostriatal Dopamine Pathway: Habit Formation Page 37 11/18/15 2:49:20 PM
38 Own-Happy > Unknown-Happy Normative Mothers (n=36) Addicted Mothers (n=39) VENTRO- MEDIAL PFC Time (sec) Time (sec) VENTRAL STRIATUM Time (sec) Time (sec) Page 38 11/18/15 2:49:20 PM
39 Own-Happy > Unknown-Happy Normative Mothers (n=36) x = -7 Addicted Mothers (n=39) x = -16 VENTRO- MEDIAL PFC Time (sec) Time (sec) y = 7 y = 7 VENTRAL STRIATUM Time (sec) Time (sec) Page 39 11/18/15 2:49:20 PM
40 Own-Happy Unknown-Happy > Normative Mothers (n=36) Addicted Mothers (n=39) y = 1 HYPOTHALAMUS Time (sec) Time (sec) Own-Happy Unknown-Happy Page 40 11/18/15 2:49:20 PM
41 Own-Happy > Unknown-Happy Decreased brain response to owninfant in addicted mothers z = Own-Happy Unknown-Happy vmpfc VS p < Hypothalamus Hypothalamus R VS L VS R vmpfc L vmpfc Page 41 11/18/15 2:49:21 PM
42 Where to from here? Randomized controlled trials of intranasal oxytocin - Mothers with addiction - Post-natal depression - Mothers with insecure attachment Comparing maternal brain and oxytocin responses in mothers with or without obesity Page 42 11/18/15 2:49:21 PM
43 INTRANASAL OXYTOCIN VENTROMEDIAL PREFRONTAL CORTEX DORSOLATERAL PREFRONTAL CORTEX SENSORY INPUT (e.g. child face/cry cues) VENTRAL STRIATUM + + AMYGDALA DORSAL STRIATUM + + +/- +/- MOTOR OUTPUT (e.g. caregiving behavior) HYPO- THALAMUS ENDOGENOUS OXYTOCIN VENTRAL TEGMENTAL AREA + SUBSTANTIA NIGRA Mesocorticolimbic Dopamine Pathway: Reward Nigrostriatal Dopamine Pathway: Habit Formation Page 43 11/18/15 2:49:21 PM
44 Oxytocin increases reward and amygdala response to infant faces Own-Happy > Unknown-Happy Normative Mothers (n=10) Oxytocin Placebo VENTRAL/DO RSAL STRIATUM AMYGDALA VENTRAL TEGMENTAL AREA (VTA) Page 44 11/18/15 2:49:21 PM
45 Oxytocin increases reward and amygdala response to infant faces in addicted mothers Own-Happy > Unknown-Happy Addicted Mothers (n=3) Oxytocin Placebo DORSAL STRIATUM AMYGDALA Page 45 11/18/15 2:49:21 PM
46 In Summary Children who are exposed to early life adversity, including abuse and neglect, are at greater risk of developing addiction problems Unresolved trauma is almost universally seen in mothers with substance addictions Addiction and early life adversity may impair a mother s ability to provide sensitive caregiving of her offspring, via reduced processing of natural reward cues in the brain Oxytocin may help to ameliorate some of these effects. Page 46 11/18/15 2:49:22 PM
47 Acknowledgements Attachment and Neurodevelopment Lab members - Sohye Kim, Research Associate - Udita Iyengar, Graduate Student - Sheila Martinez, Ana Sanchez, and Leah Sanchez, Research Assistants Peter Fonagy, University College London Collaborators at Yale Child Study Center: Linda Mayes, Helena Rutherford, Marc Potenza NIH Grant Support: NICHD K23 HD43097 and R01 HD065819; K12 HD41648 Baylor Child Health Research Center: Mentored Research Program; NIDA R01 DA USDA CRIS grant D Follow us on Facebook: AttachmentNeurodevelopmentLab Page 47 11/18/15 2:49:22 PM
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