Attachment in the brain: adult attachment representations predict amygdala and behavioral responses to infant crying

Current research found that adult attachment representations influence neural, emotional, and behavioral responses to infant crying, thus validating the Berkeley Adult Attachment Interview with functional Magnetic Resonance Imaging. This study examined amygdala activation, feelings of irritation, and the use of excessive force as indicated by grip strength using a handgrip dynamometer during exposure to infant crying and scrambled control sounds in 21 women without children. Individuals with insecure attachment representations showed heightened amygdala activation when exposed to infant crying compared to individuals with secure attachment representations. In addition, insecure individuals experienced more irritation during infant crying and used more excessive force than individuals with a secure representation. Amygdala hyperactivity might be one of the mechanisms underlying the experience of negative emotions during exposure to infant crying in insecure individuals and might explain why insecure parents respond inconsistently to infant signals or reject their infants' attachment behavior.

[1]  Christian Büchel,et al.  Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans , 2010, Proceedings of the National Academy of Sciences.

[2]  R. Trent,et al.  Age-related incidence curve of hospitalized Shaken Baby Syndrome cases: convergent evidence for crying as a trigger to shaking. , 2006, Child abuse & neglect.

[3]  R. Kobak,et al.  Psychophysiology in attachment interviews: converging evidence for deactivating strategies. , 1992, Child development.

[4]  E. Waters,et al.  The stability of attachment security from infancy to adolescence and early adulthood: general introduction. , 2000, Child development.

[5]  Maarten A. S. Boksem,et al.  Oxytocin Modulates Amygdala, Insula, and Inferior Frontal Gyrus Responses to Infant Crying: A Randomized Controlled Trial , 2011, Biological Psychiatry.

[6]  P. S. Zeskind,et al.  The Perceptions of Infant Distress Signals Varying in Pitch by Cocaine-using Mothers , 2003 .

[7]  M. Bakermans-Kranenburg,et al.  The first 10,000 Adult Attachment Interviews: distributions of adult attachment representations in clinical and non-clinical groups , 2009, Attachment & human development.

[8]  J. Hirsch,et al.  Distinct but overlapping neural networks subserve depression and insecure attachment. , 2012, Social cognitive and affective neuroscience.

[9]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[10]  P. Levitt,et al.  Amygdala Gene Expression Correlates of Social Behavior in Monkeys Experiencing Maternal Separation , 2007, The Journal of Neuroscience.

[11]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[12]  T. M. Horner Growing Points in Attachment Theory and Research , 1987 .

[13]  F. Seguin,et al.  Effects of stress throughout the lifespan on the brain, behaviour and cognition , 2009 .

[14]  Nancy L. McElwain,et al.  Maternal sensitivity to infant distress and nondistress as predictors of infant-mother attachment security. , 2006, Journal of family psychology : JFP : journal of the Division of Family Psychology of the American Psychological Association.

[15]  Marinus H. van IJzendoorn,et al.  The Role of Oxytocin in Mother‐Infant Relations: A Systematic Review of Human Studies , 2011, Harvard review of psychiatry.

[16]  Keith J. Worsley,et al.  Statistical analysis of activation images , 2001 .

[17]  E. Leerkes,et al.  Attachment linked predictors of women's emotional and cognitive responses to infant distress , 2006, Attachment & human development.

[18]  Glenn I. Roisman,et al.  Adults' autonomic and subjective emotional responses to infant vocalizations: the role of secure base script knowledge. , 2009, Developmental psychology.

[19]  Marinus H. van IJzendoorn,et al.  Adult attachment representations, parental responsiveness, and infant attachment: a meta-analysis on the predictive validity of the Adult Attachment Interview. , 1995, Psychological bulletin.

[20]  Harriet Oster,et al.  Parental sensitivity to infant distress: what do discrete negative emotions have to do with it? , 2012, Attachment & human development.

[21]  Orna Zagoory-Sharon,et al.  Evidence for a Neuroendocrinological Foundation of Human Affiliation , 2007, Psychological science.

[22]  M. Kringelbach The human orbitofrontal cortex: linking reward to hedonic experience , 2005, Nature Reviews Neuroscience.

[23]  Ilanit Gordon,et al.  Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact , 2010, Psychoneuroendocrinology.

[24]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[25]  Maarten A. S. Boksem,et al.  No Laughing Matter: Intranasal Oxytocin Administration Changes Functional Brain Connectivity during Exposure to Infant Laughter , 2012, Neuropsychopharmacology.

[26]  T. Hare,et al.  Elevated amygdala response to faces following early deprivation. , 2011, Developmental science.

[27]  M. Bakermans-Kranenburg,et al.  Physiological reactivity to infant crying: a behavioral genetic study , 2010, Genes, brain, and behavior.

[28]  Danielle S. Bassett,et al.  A validated network of effective amygdala connectivity , 2007, NeuroImage.

[29]  Carol Carter Porges Neuroendocrine perspectives on social attachment and love , 1998 .

[30]  M. Craske,et al.  A Specific and Rapid Neural Signature for Parental Instinct , 2008, PloS one.

[31]  M. Bakermans-Kranenburg,et al.  Oxytocin decreases handgrip force in reaction to infant crying in females without harsh parenting experiences. , 2012, Social cognitive and affective neuroscience.

[32]  J. Bowlby Attachment and loss: retrospect and prospect. , 1969, The American journal of orthopsychiatry.

[33]  Eva M. Fraedrich,et al.  Brain activity during emotion perception: the role of attachment representation , 2010, Attachment & human development.

[34]  D. Benoit,et al.  Stability and transmission of attachment across three generations. , 1994, Child development.

[35]  Gregory G. Brown,et al.  Adolescents with major depression demonstrate increased amygdala activation. , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[36]  H. Engeland,et al.  Intranasal oxytocin increases fathers’ observed responsiveness during play with their children: A double-blind within-subject experiment , 2010, Psychoneuroendocrinology.

[37]  D. Wilson,et al.  Handgrip Strength and Socially Dominant Behavior in Male Adolescents , 2010, Evolutionary psychology : an international journal of evolutionary approaches to psychology and behavior.

[38]  Marinus H. van IJzendoorn,et al.  Stability and Discriminant Validity of the Adult Attachment Interview: A Psychometric Study in Young Israeli Adults , 1994 .

[39]  Jude Cassidy,et al.  Attachment and the processing of social information across the life span: theory and evidence. , 2011, Psychological bulletin.

[40]  H. Steele,et al.  Clinical applications of the adult attachment interview , 2008 .

[41]  Peter A. Bos,et al.  Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: A review of single administration studies , 2012, Frontiers in Neuroendocrinology.

[42]  P. Fonagy,et al.  Adult attachment predicts maternal brain and oxytocin response to infant cues , 2009, Neuropsychopharmacology.

[43]  Tong-gui Li,et al.  Brain responses to facial expressions by adults with different attachment–orientations , 2008, Neuroreport.

[44]  Stephen M. Smith,et al.  Functional MRI : an introduction to methods , 2002 .

[45]  E. Macaluso,et al.  Attachment models affect brain responses in areas related to emotions and empathy in nulliparous women , 2013, Human brain mapping.

[46]  M. F. van der Wal,et al.  Infant crying and abuse , 2004, The Lancet.

[47]  L. Sroufe,et al.  Attachment from infancy to early adulthood in a high-risk sample: continuity, discontinuity, and their correlates. , 2000, Child development.

[48]  M. Main,et al.  Studying differences in language usage in recounting attachment history: An introduction to the AAI. , 2008 .

[49]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[50]  E. Hesse The Adult Attachment Interview: Protocol, method of analysis, and empirical studies. , 2008 .

[51]  John J. Skowronski,et al.  Parental responses to infant crying: the influence of child physical abuse risk and hostile priming. , 2008, Child abuse & neglect.

[52]  Patrik Vuilleumier,et al.  Individual Attachment Style Modulates Human Amygdala and Striatum Activation during Social Appraisal , 2008, PloS one.

[53]  Stephen Hughes Attachment and Loss. Vol. I , 1969, Mental Health.

[54]  Lisa M Shin,et al.  Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study , 2000, Biological Psychiatry.

[55]  R. Harmon,et al.  Security in Infancy , Childhood , and Adulthood : A Move to the Level of Representation , 2007 .

[56]  Glenn I. Roisman,et al.  The Adult Attachment Interview and self-reports of attachment style: an empirical rapprochement. , 2007, Journal of personality and social psychology.

[57]  Erich Seifritz,et al.  Differential sex-independent amygdala response to infant crying and laughing in parents versus nonparents , 2003, Biological Psychiatry.

[58]  Joseph Soltis,et al.  The signal functions of early infant crying , 2004, Behavioral and Brain Sciences.

[59]  M. Bakermans-Kranenburg,et al.  A Psychometric Study of the Adult Attachment Interview : Reliability and Discriminant Validity , 1993 .

[60]  E. Gershoff,et al.  The affective structure of supportive parenting: depressive symptoms, immediate emotions, and child-oriented motivation. , 2004, Developmental psychology.

[61]  Mark S. George,et al.  A potential role for thalamocingulate circuitry in human maternal behavior , 2002, Biological Psychiatry.

[62]  J. Coan TOWARD A NEUROSCIENCE OF ATTACHMENT , 2008 .

[63]  Pienie Zwitserlood,et al.  Reduced amygdala-prefrontal coupling in major depression: association with MAOA genotype and illness severity. , 2009, The international journal of neuropsychopharmacology.

[64]  Marinus H. van IJzendoorn Adult attachment representations, parental responsiveness, and infant attachment: a meta-analysis on the predictive validity of the adult attachment interview , 1995 .

[65]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[66]  H. Walter,et al.  Measuring Attachment Representation in an fMRI Environment: A Pilot Study , 2006, Psychopathology.

[67]  P. S. Zeskind,et al.  Relations Between Women's Depressive Symptoms and Perceptions of Infant Distress Signals Varying in Pitch. , 2001, Infancy : the official journal of the International Society on Infant Studies.

[68]  Talma Hendler,et al.  Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers , 2011, Neuropsychopharmacology.

[69]  A. Schore Effects of a secure attachment relationship on right brain development, affect regulation, and infant mental health , 2001 .

[70]  M. Bakermans-Kranenburg,et al.  Intended sensitive and harsh caregiving responses to infant crying: the role of cry pitch and perceived urgency in an adult twin sample. , 2010, Child abuse & neglect.

[71]  D. Bugental,et al.  In charge but not in control: the management of teaching relationships by adults with low perceived power. , 1999, Developmental psychology.

[72]  M. Main The Organized Categories of Infant, Child, and Adult Attachment: Flexible Vs. Inflexible Attention Under Attachment-Related Stress , 2000, Journal of the American Psychoanalytic Association.

[73]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[74]  Nicholas S. Thompson,et al.  A reassessment of the role of pitch and duration in adults' responses to infant crying. , 1998 .

[75]  Kamryn T. Eddy,et al.  Amygdala-frontal connectivity during emotion regulation. , 2007, Social cognitive and affective neuroscience.

[76]  Phillip R. Shaver,et al.  Handbook of attachment : theory, research, and clinical applications , 1999 .

[77]  D. Yurgelun-Todd,et al.  fMRI of fearful facial affect recognition in panic disorder: the cingulate gyrus-amygdala connection. , 2006, Journal of affective disorders.

[78]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[79]  T. Dix,et al.  The affective organization of parenting: adaptive and maladaptive processes. , 1991, Psychological bulletin.

[80]  M. Bakermans-Kranenburg,et al.  Stress regulation in adolescents: physiological reactivity during the adult attachment interview and conflict interaction. , 2008, Child development.

[81]  E. Waters,et al.  Discriminant validity of the adult attachment interview. , 1996, Child development.