The Intergenerational Transmission of Attachment: - IASA

The IntergenerationalTransmission ofAttachment:What the Brain Has to SayDr Lane Strathearn, FRACP PhDAssistant Professor, Department of PediatricsBaylor College of Medicine/Texas Children’s Hospital

Child Neglect• Most prevalent and rapidlyincreasing form of childmaltreatment ~40% of reported cases are forneglect• Yet, it is the least studied andmost poorly understood type ofmaltreatment

PhysicalNeglectEmotionalNeglect• Failure to provide:FoodClothingShelterMedical careEducational provision• Failure to provide:ComfortProtectionLoveDisciplineEncouragement

Consequences ofChild Neglect• Impaired cognitive development• Language delays• Increased risk of childhoodaggression• Internalizing and externalizingbehavior problems• Increased risk of subsequentabuse

IntergenerationalTransmission of Attachment• Overall, there was a 73% match ofsecure/insecure attachmentbetween mothers and infants (Χ 2 = 10.7,df = 1, κ = 0.46, p = 0.001)

IntergenerationalTransmission of Attachment65%29%Shah, Fonagy, Strathearn, 2010

IntergenerationalTransmission of Attachment65%29%• Increased likelihood of inversion ofpatterns across Type A and C groups

IntergenerationalTransmission of AttachmentMOTHER’SATTACHMENTSTRATEGYINFANT’SATTACHMENTSTRATEGY

IntergenerationalTransmission of Attachment“TRANSMISSION GAP”MOTHER’SATTACHMENTSTRATEGYMaternal sensitivityor “sensitiveresponsiveness”?Mentalizing?INFANT’SATTACHMENTSTRATEGYGeneticfactors?

IntergenerationalTransmission of AttachmentMOTHER’SATTACHMENTSTRATEGYINFANT’SATTACHMENTSTRATEGY

DOPAMINESYSTEMOXYTOCINSYSTEMPituitary GlandPeripheral blood

Maternal Behavior in the Rat• Pup vocalization• Licking andgrooming• Arched-back nursingChampagne, 2003

Oxytocin and DopamineSystems• Oxytocin “affiliation” pathways Pituitary gland Hypothalamus (MPOA, PVN)• Dopamine “reward” pathways Ventral striatum Medial prefrontal cortex• The development of these systemsappears to be strongly influenced by earlymaternal care

Neuroendocrine Systems Importantin Maternal Behavior1. Dopamine (DA)• Nucleus accumbens - DAimportant in rat maternalbehavior and releasedduring mother-pupinteraction• Important factor in cognitivedevelopment andestablishing reward-basedcontingencies2. Oxytocin• Central hormone critical for the social andmaternal behavior,• Social memory;• Anxiolytic properties

Oxytocin and maternalcaregiving• In animal models of maternal care,oxytocin is critical for the initiation ofmaternal care• In ewes, oxytocin results in selectivebonding with the lamb• Oxytocin neurons may also connectwith the brain’s dopamine “reward”system, resulting in changes in “longtermconditioned preferences”

Oxytocin and maternalcaregiving• Oxytocin is a peripheral hormoneimportant in childbirth and lactation• Breastfeeding/suckling stimulates itsproduction• It also has important central effects inthe brain to help prepare for longtermchild rearing• “Calm and connection” effect

DNA Methylation and Epigenetics• Early life somatosensory stimulation(“pup licking”) results in: Change in methylation pattern at stressreceptor gene, resulting in a reducedstress response Change in methylation pattern forestrogen receptor gene, resulting inchanges in oxytocin functioning, andenhanced maternal caregiving behavior infemale offspring Enhanced dopamine production inresponse to infant cues

IntergenerationalTransmission of AttachmentMOTHER’SATTACHMENTSTRATEGYINFANT’SATTACHMENTSTRATEGY

IntergenerationalTransmission of AttachmentMOTHER’SATTACHMENTSTRATEGYINFANT’SATTACHMENTSTRATEGY

Study OutlineVisit 1:PregnancyVisit 2:VideotapingVisit 3:ScanningVisit 4:Follow-Up3 rd trimester 7 mths 10 mths14 mthsStudyTimelineBIRTH20 min 5 min 6 min 20 minMother-infantseparation 1“Free play”interactionMirror-basedinteractionMotherinfantseparation 2DataCollected•AAI•Demographics•PDQ•BDI•PANAS (1)•Demographics•ATQ•Infant faceimagesBlood draws•Oxytocin•Cortisol•Adrenaline•Noradrenaline•PANAS (2)•IBQ•PSI•WTAR•Breastfeedingduration•Hours separatedper week•Bayley Scalesof InfantDevelopment•StrangeSituationProcedureStrathearn L, et al. Neuropsychopharmacology. 2009.

Visit 1: PregnancyVisit 1:PregnancyVisit 2:VideotapingVisit 3:ScanningVisit 4:Follow-Up3 rd trimester 7 mths 10 mths14 mthsStudyTimelineBIRTH20 min 5 min 6 min 20 minMother-infantseparation 1“Free play”interactionMirror-basedinteractionMotherinfantseparation 2DataCollected•AAI•Demographics•PDQ•BDI•PANAS (1)•Demographics•ATQ•Infant faceimagesBlood draws•Oxytocin•Cortisol•Adrenaline•Noradrenaline•PANAS (2)•IBQ•PSI•WTAR•Breastfeedingduration•Hours separatedper week•Bayley Scalesof InfantDevelopment•StrangeSituationProcedureAAIStrathearn L, et al. Neuropsychopharmacology. 2009.

Visit 2: VideotapingVisit 1:PregnancyVisit 2:VideotapingVisit 3:ScanningVisit 4:Follow-Up3 rd trimester 7 mths 10 mths14 mthsStudyTimelineBIRTH20 min 5 min 6 min 20 minMother-infantseparation 1“Free play”interactionMirror-basedinteractionMotherinfantseparation 2DataCollected•AAI•Demographics•PDQ•BDI•PANAS (1)•Demographics•ATQ•Infant faceimagesBlood draws•Oxytocin•Cortisol•Adrenaline•Noradrenaline•PANAS (2)•IBQ•PSI•WTAR•Breastfeedingduration•Hours separatedper week•Bayley Scalesof InfantDevelopment•StrangeSituationProcedureAAI

Visit 3: fMRI ScanningVisit 1:PregnancyVisit 2:VideotapingVisit 3:ScanningVisit 4:Follow-Up3 rd trimester 7 mths 10 mths14 mthsStudyTimelineBIRTH20 min 5 min 6 min 20 minMother-infantseparation 1“Free play”interactionMirror-basedinteractionMotherinfantseparation 2DataCollected•AAI•Demographics•PDQ•BDI•PANAS (1)•Demographics•ATQ•Infant faceimagesBlood draws•Oxytocin•Cortisol•Adrenaline•Noradrenaline•PANAS (2)•IBQ•PSI•WTAR•Breastfeedingduration•Hours separatedper week•Bayley Scalesof InfantDevelopment•StrangeSituationProcedureAAI

Visit 4: Follow-UpVisit 1:PregnancyVisit 2:VideotapingVisit 3:ScanningVisit 4:Follow-Up3 rd trimester 7 mths 10 mths14 mthsStudyTimelineBIRTH20 min 5 min 6 min 20 minMother-infantseparation 1“Free play”interactionMirror-basedinteractionMotherinfantseparation 2DataCollected•AAI•Demographics•PDQ•BDI•PANAS (1)•Demographics•ATQ•Infant faceimagesBlood draws•Oxytocin•Cortisol•Adrenaline•Noradrenaline•PANAS (2)•IBQ•PSI•WTAR•Breastfeedingduration•Hours separatedper week•Bayley Scalesof InfantDevelopment•StrangeSituationProcedureAAIBRAIN / BEHAVIORSSP

Three Affective StatesCrying Neutral Smiling

2 sec2 sec2 secOwn:Happy(‏OH‏)‏Unknown:Happy(‏UH‏)‏Unknown:Sad(‏US‏)‏2 sec2 sec2 sec2–6 sec randominter-stimulusintervalOwn:Neutral(‏ON‏)‏Unknown:Neutral(‏UN‏)‏Own:Sad(‏OS‏)‏

2 sec2 sec2 secAFFECTSTIMULUSTYPESHappyNeutralSadIDENTITYOwnInfantOHONOSUnknownInfantUHUNUSOwn:Happy(‏OH‏)‏Unknown:Happy(‏UH‏)‏Unknown:Sad(‏US‏)‏2 sec2 sec2 sec2–6 sec randominter-stimulusintervalOwn:Neutral(‏ON‏)‏Unknown:Neutral(‏UN‏)‏Own:Sad(‏OS‏)‏

Functional MagneticResonance Imaging (fMRI)fMRI allows for the time course of human brain activity tobe imaged.

The Hemodynamic ResponseNeural pathwayHemodynamicsMR scannerFigure adapted from Chein & Schneider

Initial FindingsVentral striatumCingulate CortexSubstantia nigraVTAn=28, p

A. Dorsal striatumB. Substantia nigra

A. Dorsal striatumB. Substantia nigra

fMRI response (% BOLD signal +/- se)A. Dorsal striatumHAPPY0.40.30.2***0.10-0.1-0.2-0.3-0.4Time (sec)Own baby faceUnknown baby faceB. Substantia nigra

fMRI response (% BOLD signal +/- se)A. Dorsal striatumHAPPYNEUTRAL0.40.30.20.1*** *0-0.1-0.2-0.3-0.4Time (sec)Own baby faceUnknown baby faceB. Substantia nigra

fMRI response (% BOLD signal +/- se)A. Dorsal striatumHAPPY NEUTRAL SAD0.40.30.20.1*** *0-0.1-0.2-0.3-0.4Time (sec)Own baby faceUnknown baby faceB. Substantia nigra

fMRI response (% BOLD signal +/- se)A. Dorsal stiatumHAPPY NEUTRAL SAD0.40.30.20.1*** *0-0.1-0.2-0.3-0.40.40.30.2***0.10-0.1-0.2-0.3-0.4-4 -2 0 2 4 6 8 10 12Time (sec)B. Substantia nigraOwn baby faceUnknown baby face

fMRI response (% BOLD signal +/- se)A. Dorsal striatumHAPPY NEUTRAL SAD0.40.30.2*** *0.10-0.1-0.2-0.3-0.40.40.30.2****0.10-0.1-0.2-0.3-0.4-4 -2 0 2 4 6 8 10 12 -4 -2 0 2 4 6 8 10 12Time (sec)B. Substantia nigraOwn baby faceUnknown baby face

fMRI response (% BOLD signal +/- se)A. Dorsal striatumHAPPY NEUTRAL SAD0.40.30.2*** *0.10-0.1-0.2-0.3-0.40.40.30.2****0.10-0.1-0.2-0.3-0.4-4 -2 0 2 4 6 8 10 12 -4 -2 0 2 4 6 8 10 12Time (sec)-4 -2 0 2 4 6 8 10 12B. Substantia nigraOwn baby faceUnknown baby face

Attachment Theory• Originally formulated by JohnBowlby in 1969• Innate biological system to ensureprotection and reproduction• Individual differences in attachment“security” are associated withmaternal care and infantsocial/emotional development

Group Comparisons• Comparison of 15 “secure” mothers and15 “insecure/dismissing”• No significant group differences wereseen, with respect to: Maternal SES, race, education or IQ Self-reported parenting stress Pre- or post-natal depression orpsychopathology risk Mother or infant temperament Infant development at 14 months Breastfeeding duration

Secure vs.Insecure/DismissingSECURE Medial PFC Orbitofrontalcortex Ventral striatumINSECURE /DISMISSING Dorsolateral PFC

% Signal Change% Signal ChangeOwn Happy Faces:Secure vs. Insecure AttachmentBilateralVentralStriatumVS54321(se=1.0, t=3.0, p=0.006)0y=11-1SecureInsecure/DismissingmPFC1.51(se=0.4, t=3.1, p=0.005)0.5RightMedialPFCx=-60-0.5-1-1.5SecureInsecure/DismissingStrathearn L, Fonagy P, Amico J, Montague PR. Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology. 2009. [Epub ahead ofprint].

Secure vs.Insecure/DismissingSECURE Medial PFC Orbitofrontalcortex Ventral striatum Ventral striatumINSECURE /DISMISSING Dorsolateral PFC Dorsolateral PFC Anterior insula

Strathearn L, Fonagy P, Amico J, Montague PR. Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology. 2009. [Epub aheadprint].% Signal Change% Signal ChangeOwn Sad Faces:Secure vs. Insecure Attachment1.4R VentralStriatumVSVS1.210.80.60.4(se=0.4, t=3.1, p=0.005)0.20-0.2-0.4y=11y=11-0.6SecureInsecure/DismissingInsula1.210.8(se=1.0, t=3.0, p=0.006)0.60.4R Insula0.20-0.2y=17x=-6-0.4SecureInsecure/Dismissing

(‏pg/ml‏)‏ Serum oxytocinChange in peripheral oxytocinwith mother-infant interaction2.32.11.91.7*Type B (Secure)Type A(Insecure/Dismissing)1.51.31.1* P

Own > Unknown Faces:Oxytocin ResponseHypothalamus/Pituitary Region>Hypothalamus/Hypothalamus/Pituitary RegionPituitary Regionr s =0.60,P=0.001(-3,2,-16)Strathearn L, Fonagy P, Amico J, Montague PR. Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology. 2009. [Epub ahead of

Oxytocin Response andVentral Striatum ActivationVentralStriatumactivationStrathearn L, Fonagy P, Amico J, Montague PR. Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology. 2009. [Epub ahead of print].

Adjusted frequency ofattuned vocalizationsMarked, attuned non-imitativematernal vocalizations

Adjusted frequency ofattuned vocalizationsMarked, attuned non-imitativematernal vocalizations

Modified Still-Face

IntergenerationalTransmission of Attachment• Type B mothers Have increased dopamine rewardresponses in the brain on seeingtheir infant’s face Have increased oxytocin responseon interacting with their infant Are more attuned in their vocalcommunication with their infantAre more likely to have Type Bchildren

• Type A mothers Have decreased dopamine rewardresponses in the brain on seeing theirinfant’s happy face Have insula activation in response to theirinfant’s crying face Have less oxytocin response oninteracting with their infant Are less attuned in their vocalcommunication with their infantIntergenerationalTransmission of AttachmentAre more likely to have Type C children

Future Directions: ExploringEmotional NeglectR I S K F O R E M O T I O N A L N E G L E C TInsecure/DismissingAdult AttachmentDopamine andoxytocinEFFECTS OFINTRANASALOXYTOCINMaternal Responses toInfant Cues1.Brain•Functional MRI•Eye gaze tracking2.Behavior•Videotaped free play•Modified Still-Face paradigmIndirect Measures of Maternal Emotional Neglect•Reduced brain reward activation to infant faces•Reduced eye gaze when viewing sad infant faces•Reduced maternal sensitivity•Reduced contingent responses to infant cues

Acknowledgements• Dr Michael O’Callaghan, Prof Jake Najmanand the Mater-University Study of Pregnancy• Peter Fonagy, UCL• Families, Youth and Community CareQueensland, Australia• Child Protection Information Systems,Brisbane, Australia• Read Montague, Samuel McClure at theHuman Neuroimaging Laboratory, BaylorCollege of Medicine