Literature DB >> 24637261

Approaching the biology of human parental attachment: brain imaging, oxytocin and coordinated assessments of mothers and fathers.

J E Swain1, P Kim2, J Spicer3, S S Ho4, C J Dayton5, A Elmadih6, K M Abel6.   

Abstract

Brain networks that govern parental response to infant signals have been studied with imaging techniques over the last 15 years. The complex interaction of thoughts and behaviors required for sensitive parenting enables the formation of each individual's first social bonds and critically shapes development. This review concentrates on magnetic resonance imaging experiments which directly examine the brain systems involved in parental responses to infant cues. First, we introduce themes in the literature on parental brain circuits studied to date. Next, we present a thorough chronological review of state-of-the-art fMRI studies that probe the parental brain with a range of baby audio and visual stimuli. We also highlight the putative role of oxytocin and effects of psychopathology, as well as the most recent work on the paternal brain. Taken together, a new model emerges in which we propose that cortico-limbic networks interact to support parental brain responses to infants. These include circuitry for arousal/salience/motivation/reward, reflexive/instrumental caring, emotion response/regulation and integrative/complex cognitive processing. Maternal sensitivity and the quality of caregiving behavior are likely determined by the responsiveness of these circuits during early parent-infant experiences. The function of these circuits is modifiable by current and early-life experiences, hormonal and other factors. Severe deviation from the range of normal function in these systems is particularly associated with (maternal) mental illnesses - commonly, depression and anxiety, but also schizophrenia and bipolar disorder. Finally, we discuss the limits and extent to which brain imaging may broaden our understanding of the parental brain given our current model. Developments in the understanding of the parental brain may have profound implications for long-term outcomes in families across risk, resilience and possible interventions. This article is part of a Special Issue entitled Oxytocin and Social Behav.
Copyright © 2014 Elsevier B.V. All rights reserved.

Entities:  

Keywords:  Attachment; Brain imaging; Caregiving; Maternal; Oxytocin; Parenting; Parent–child relationship; Paternal; fMRI

Mesh:

Substances:

Year:  2014        PMID: 24637261      PMCID: PMC4157077          DOI: 10.1016/j.brainres.2014.03.007

Source DB:  PubMed          Journal:  Brain Res        ISSN: 0006-8993            Impact factor:   3.252


  194 in total

Review 1.  The neurobiology of attachment.

Authors:  T R Insel; L J Young
Journal:  Nat Rev Neurosci       Date:  2001-02       Impact factor: 34.870

2.  Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors.

Authors:  F Champagne; J Diorio; S Sharma; M J Meaney
Journal:  Proc Natl Acad Sci U S A       Date:  2001-10-16       Impact factor: 11.205

3.  The nature of the mother's tie to her infant: maternal bonding under conditions of proximity, separation, and potential loss.

Authors:  R Feldman; A Weller; J F Leckman; J Kuint; A I Eidelman
Journal:  J Child Psychol Psychiatry       Date:  1999-09       Impact factor: 8.982

4.  Maternal responsiveness and children's achievement of language milestones.

Authors:  C S Tamis-LeMonda; M H Bornstein; L Baumwell
Journal:  Child Dev       Date:  2001 May-Jun

Review 5.  Preoccupations and behaviors associated with romantic and parental love. Perspectives on the origin of obsessive-compulsive disorder.

Authors:  J F Leckman; L C Mayes
Journal:  Child Adolesc Psychiatr Clin N Am       Date:  1999-07

6.  The relations of regulation and emotionality to children's externalizing and internalizing problem behavior.

Authors:  N Eisenberg; A Cumberland; T L Spinrad; R A Fabes; S A Shepard; M Reiser; B C Murphy; S H Losoya; I K Guthrie
Journal:  Child Dev       Date:  2001 Jul-Aug

7.  Early parental preoccupations and behaviors and their possible relationship to the symptoms of obsessive-compulsive disorder.

Authors:  J F Leckman; L C Mayes; R Feldman; D W Evans; R A King; D J Cohen
Journal:  Acta Psychiatr Scand Suppl       Date:  1999

8.  Oxytocin responsivity in mothers of infants: a preliminary study of relationships with blood pressure during laboratory stress and normal ambulatory activity.

Authors:  K C Light; T E Smith; J M Johns; K A Brownley; J A Hofheimer; J A Amico
Journal:  Health Psychol       Date:  2000-11       Impact factor: 4.267

9.  Feasibility of using fMRI to study mothers responding to infant cries.

Authors:  J P Lorberbaum; J D Newman; J R Dubno; A R Horwitz; Z Nahas; C C Teneback; C W Bloomer; D E Bohning; D Vincent; M R Johnson; N Emmanuel; O Brawman-Mintzer; S W Book; R B Lydiard; J C Ballenger; M S George
Journal:  Depress Anxiety       Date:  1999       Impact factor: 6.505

10.  Frightening maternal behavior linking unresolved loss and disorganized infant attachment.

Authors:  C Schuengel; M J Bakermans-Kranenburg; M H Van IJzendoorn
Journal:  J Consult Clin Psychol       Date:  1999-02
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  75 in total

1.  Depression alters maternal extended amygdala response and functional connectivity during distress signals in attachment relationship.

Authors:  S Shaun Ho; James E Swain
Journal:  Behav Brain Res       Date:  2017-03-02       Impact factor: 3.332

Review 2.  Family Accommodation of Child and Adolescent Anxiety: Mechanisms, Assessment, and Treatment.

Authors:  Kaila R Norman; Wendy K Silverman; Eli R Lebowitz
Journal:  J Child Adolesc Psychiatr Nurs       Date:  2015-08-04

3.  Parent-child intervention decreases stress and increases maternal brain activity and connectivity during own baby-cry: An exploratory study.

Authors:  James E Swain; S Shaun Ho; Katherine L Rosenblum; Diana Morelen; Carolyn J Dayton; Maria Muzik
Journal:  Dev Psychopathol       Date:  2017-05

4.  Dopamine in the medial amygdala network mediates human bonding.

Authors:  Shir Atzil; Alexandra Touroutoglou; Tali Rudy; Stephanie Salcedo; Ruth Feldman; Jacob M Hooker; Bradford C Dickerson; Ciprian Catana; Lisa Feldman Barrett
Journal:  Proc Natl Acad Sci U S A       Date:  2017-02-13       Impact factor: 11.205

5.  Neural plasticity in fathers of human infants.

Authors:  Pilyoung Kim; Paola Rigo; Linda C Mayes; Ruth Feldman; James F Leckman; James E Swain
Journal:  Soc Neurosci       Date:  2014-06-24       Impact factor: 2.083

6.  Adults' implicit associations to infant positive and negative acoustic cues: Moderation by empathy and gender.

Authors:  Vincenzo Paolo Senese; Paola Venuti; Francesca Giordano; Maria Napolitano; Gianluca Esposito; Marc H Bornstein
Journal:  Q J Exp Psychol (Hove)       Date:  2016-07-28       Impact factor: 2.143

7.  Socioeconomic disadvantages and neural sensitivity to infant cry: role of maternal distress.

Authors:  Pilyoung Kim; Christian Capistrano; Christina Congleton
Journal:  Soc Cogn Affect Neurosci       Date:  2016-05-05       Impact factor: 3.436

8.  Implicit association to infant faces: Genetics, early care experiences, and cultural factors influence caregiving propensities.

Authors:  Vincenzo Paolo Senese; Kazuyuki Shinohara; Gianluca Esposito; Hirokazu Doi; Paola Venuti; Marc H Bornstein
Journal:  Behav Brain Res       Date:  2016-09-17       Impact factor: 3.332

9.  Maternal brain resting-state connectivity in the postpartum period.

Authors:  Alexander J Dufford; Andrew Erhart; Pilyoung Kim
Journal:  J Neuroendocrinol       Date:  2019-06-14       Impact factor: 3.627

10.  Early Parenting Intervention Effects on Brain Responses to Maternal Cues Among High-Risk Children.

Authors:  Emilio A Valadez; Nim Tottenham; Alexandra R Tabachnick; Mary Dozier
Journal:  Am J Psychiatry       Date:  2020-07-31       Impact factor: 18.112

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