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Brain activity and infant attachment history in young men during loss and reward processing

Published online by Cambridge University Press:  12 April 2017

Karina Quevedo ,
Theodore E. A. Waters ,
Hannah Scott ,
Glenn I. Roisman ,
Daniel S. Shaw  and
Erika E. Forbes
Karina Quevedo*
Affiliation:
University of Minnesota
Theodore E. A. Waters
Affiliation:
New York University Abu Dhabi
Hannah Scott
Affiliation:
University of Minnesota
Glenn I. Roisman
Affiliation:
University of Minnesota
Daniel S. Shaw
Affiliation:
University of Pittsburgh
Erika E. Forbes
Affiliation:
University of Pittsburgh
*
Address correspondence and reprint requests to: Karina Quevedo, Division of Child and Adolescent Psychiatry, Room F260, University of Minnesota, Department of Psychiatry, 2450 Riverside Avenue, Minneapolis, MN 55454; E-mail: queve001@umn.edu.
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Abstract

There is now ample evidence that the quality of early attachment experiences shapes expectations for supportive and responsive care and ultimately serves to scaffold adaptation to the salient tasks of development. Nonetheless, few studies have identified neural mechanisms that might give rise to these associations. Using a moderately large sample of low-income male participants recruited during infancy (N = 171), we studied the predictive significance of attachment insecurity and disorganization at age 18 months (as measured in the Strange Situation Procedure) for patterns of neural activation to reward and loss at age 20 years (assessed during a reward-based task as part of a functional magnetic resonance imaging scan). Results indicated that individuals with a history of insecure attachment showed hyperactivity in (a) reward- and emotion-related (e.g., basal ganglia and amygdala) structures and (b) emotion regulation and self-referential processing (cortical midline structures) in response to positive and negative outcomes (and anticipation of those outcomes). Further, the neural activation of individuals with a history of disorganized attachment suggested that they had greater emotional reactivity in anticipation of reward and employed greater cognitive control when negative outcomes were encountered. Overall, results suggest that the quality of early attachments has lasting impacts on brain function and reward processing.

Type
Special Issue Articles
Information
Development and Psychopathology , Volume 29 , Special Issue 2: Attachment in the Context of Atypical Caregiving: Harnessing Insights From a Developmental Psychopathology Perspective , May 2017 , pp. 465 - 476
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

This research was supported by K01MH092601 (to K.Q.) and grants from the National Institute on Drug Abuse (Grant 25630 to D.S.S.) and (Grant 26222 to D.S.S. and E.E.F.). We are grateful to Dr. Kathleen Thomas and Dr. Mary Phillips, key mentors and supporter of the first author's K award and progress.

References

Ainsworth, M. S., Blehar, M. C., Waters, E., & Wall, S. (1978). Patterns of attachment: A psychological study of the strange situation. Oxford: Erlbaum.Google Scholar
Anders, S., Eippert, F., Weiskopf, N., & Veit, R. (2008). The human amygdala is sensitive to the valence of pictures and sounds irrespective of arousal: An fMRI study. Social Cogntive Affective Neuroscience, 3, 233–243.CrossRefGoogle Scholar
Balleine, B. W., & Killcross, S. (2006). Parallel incentive processing: An integrated view of amygdala function. Trends in Neuroscience, 29, 272–279.CrossRefGoogle ScholarPubMed
Bernier, A., Matte-Gagne, C., Belanger, M. E., & Whipple, N. (2014). Taking stock of two decades of attachment transmission gap: Broadening the assessment of maternal behavior. Child Development, 85, 1852–1865.Google Scholar
Bowlby, J. (1980). Attachment and loss. New York: Basic Books. (Original work published 1969)Google Scholar
Bush, G., Vogt, B. A., Holmes, J., Dale, A. M., Greve, D., Jenike, M. A., & Rosen, B. R. (2002). Dorsal anterior cingulate cortex: A role in reward-based decision making. Proceedings of the National Academy of Science, 99, 523–528.Google Scholar
Cassidy, J. (1994). Emotion regulation: Influences of attachment relationships. Monographs of the Society for Research in Child Development, 59(2–3), 228–249.Google Scholar
Cassidy, J., & Shaver, P. R. (Eds.). (2008). Handbook of attachment: Theory, research, and clinical applications (2nd ed.). New York: Guilford Press.Google Scholar
Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129(Pt. 3), 564–583.Google Scholar
Cunningham, W. A., Brosch, T. (2012). Motivational salience amygdala tuning from traits, needs, values, and goals. Current Directions in Psychological Science, 21, 54–59.Google Scholar
Delgado, M. R., Nystrom, L. E., Fissell, C., Noll, D. C., & Fiez, J. A. (2000). Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology, 84, 3072–3077.Google Scholar
Farrer, C., & Frith, C. D. (2002). Experiencing oneself vs another person as being the cause of an action: The neural correlates of the experience of agency. NeuroImage, 15, 596–603.CrossRefGoogle ScholarPubMed
Fearon, R. P., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Lapsley, A. M., & Roisman, G. I. (2010). The significance of insecure attachment and disorganization in the development of children's externalizing behavior: A meta-analytic study. Child Development, 81, 435–456.Google Scholar
Forbes, E. E., Hariri, A. R., Martin, S. L., Silk, J. S., Moyles, D. L., Fisher, P. M., … Dahl, R. E. (2009). Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. American Journal of Psychiatry, 166, 64–73.Google Scholar
Forbes, E. E., Miller, A., Cohn, J. F., Fox, N. A., & Kovacs, M. (2005). Affect-modulated startle in adults with childhood-onset depression: Relations to bipolar course and number of lifetime depressive episodes. Psychiatry Research, 134, 11–25.Google Scholar
Forbes, E. E., Shaw, D. S., & Dahl, R. E. (2007). Alterations in reward-related decision making in boys with recent and future depression. Biological Psychiatry, 61, 633–639.Google Scholar
Gander, M., & Buchheim, A. (2015). Attachment classification, psychophysiology and frontal EEG asymmetry across the lifespan: A review. Frontiers of Human Neuroscience, 9, 79.CrossRefGoogle ScholarPubMed
Goel, V., & Dolan, R. J. (2001). Functional neuroanatomy of three-term relational reasoning. Neuropsychologia, 39, 901–909.Google Scholar
Grahn, J. A., Parkinson, J. A., & Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Progress in Neurobiology, 86, 141–155.Google Scholar
Groh, A. M., Fearon, R. P., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Steele, R. D., & Roisman, G. I. (2014). The significance of attachment security for children's social competence with peers: A meta-analytic study. Attachment & Human Development, 16, 103–136.Google Scholar
Groh, A. M., Roisman, G. I., Haydon, K. C., Bost, K., McElwain, N., Garcia, L., & Hester, C. (2014). Mothers’ electrophysiological, subjective, and observed emotional responding to infant crying: The role of secure base script knowledge. Development and Psychopathology. Advance online publication.Google Scholar
Groh, A. M., Roisman, G. I., van IJzendoorn, M. H., Bakermans-Kranenburg, M. J., & Fearon, R. P. (2012). The significance of insecure and disorganized attachment for children's internalizing symptoms: A meta-analytic study. Child Development, 83, 591–610.Google Scholar
Kensinger, E. A., & Schacter, D. L. (2006). Amygdala activity is associated with the successful encoding of item, but not source, information for positive and negative stimuli. Journal of Neuroscience, 26, 2564–2570.Google Scholar
Kobayakawa, M., & Kawamura, M. (2011). Neural and cognitive correlates of social cognition: Findings on neuropsychological and neuroimaging studies. Brain Nerve, 63, 1352–1360.Google Scholar
Koechlin, E., & Hyafil, A. (2007). Anterior prefrontal function and the limits of human decision-making. Science, 318, 594–598.Google Scholar
Lemche, E., Giampietro, V. P., Surguladze, S. A., Amaro, E. J., Andrew, C. M., Williams, S. C., & Phillips, M. L. (2006). Human attachment security is mediated by the amygdala: Evidence from combined fMRI and psychophysiological measures. Human Brain Mapping, 27, 623–635.Google Scholar
Luking, K. R., & Barch, D. M. (2013). Candy and the brain: Neural response to candy gains and losses. Cognitive Affective & Behavioral Neuroscience, 13, 437–451.Google Scholar
MacDonald, A. W. III, Cohen, J. D., Stenger, V. A., & Carter, C. S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288, 1835–1838.Google Scholar
Madigan, S., Atkinson, L., Laurin, K., & Benoit, D. (2013). Attachment and internalizing behavior in early childhood: A meta-analysis. Developmental Psychology, 49, 672–689.Google Scholar
Main, M., & Hesse, E. (1990). Parents’ unresolved traumatic experiences are related to infant disorganized attachment status: Is frightened and/or frightening parental behavior the linking mechanism? In Greenberg, M. T., Cicchetti, D., & Cummings, E. M. (Eds.)., Attachment in the preschool years: Theory, research, and intervention. Chicago: University of Chicago Press.Google Scholar
McGaugh, J. L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience, 27, 1–28.Google Scholar
Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: A network model of insula function. Brain Structure and Function, 214, 655–667.Google Scholar
Mikulincer, M., & Shaver, P. R. (2008). Adult attachment and affect regulation In Cassidy, J. & Shaver, P. R. (Eds.), Handbook of attachment: Theory, research, and clinical applications (pp. 503–531). New York: Guilford Press.Google Scholar
Mikulincer, M., Shaver, P. R., & Pereg, D. (2003). Attachment theory and affect regulation: The dynamics, development, and cognitive consequences of attachment-related strategies. Motivation and Emotion, 27, 77–102.CrossRefGoogle Scholar
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167–202.Google Scholar
Morgan, J. K., Shaw, D. S., & Forbes, E. E. (2014). Maternal depression and warmth during childhood predict age 20 neural response to reward. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 108–117.Google Scholar
Moutsiana, C., Fearon, P., Murray, L., Cooper, P., Goodyer, I., Johnstone, T., & Halligan, S. (2014). Making an effort to feel positive: Insecure attachment in infancy predicts the neural underpinnings of emotion regulation in adulthood. Journal of Child Psychology and Psychiatry, 55, 999–1008.Google Scholar
Murray, L. (1992). The impact of postnatal depression on infant development. Journal of Child Psychology and Psychiatry, 33, 543–561.Google Scholar
Packard, M. G., & Knowlton, B. J. (2002). Learning and memory functions of the basal ganglia. Annual Review of Neuroscience, 25, 563–593.Google Scholar
Petrides, M. (2005). Lateral prefrontal cortex: Architectonic and functional organization. Philosophical Transactions of the Royal Society of London B, 360, 781–795.Google Scholar
Quevedo, K., Johnson, A. E., Loman, M. M., Lafavor, T., Moua, B., & Gunnar, M. R. (2015). The impact of early neglect on defensive and appetitive physiology during the pubertal transition: A study of startle and postauricular reflexes. Developmental Psychobiology, 57, 289–304.Google Scholar
Riem, M. M., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Out, D., & Rombouts, S. A. (2012). Attachment in the brain: Adult attachment representations predict amygdala and behavioral responses to infant crying. Attachment & Human Development, 14, 533–551.Google Scholar
Shaw, D. S., Gilliom, M., Ingoldsby, E. M., & Nagin, D. S. (2003). Trajectories leading to school-age conduct problems. Developmental Psychology, 39, 189–200.Google Scholar
Strathearn, L., Fonagy, P., Amico, J., & Montague, P. R. (2009). Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology, 34, 2655–2666.CrossRefGoogle ScholarPubMed
Strathearn, L., Li, J., Fonagy, P., & Montague, P. R. (2008). What's in a smile? Maternal brain responses to infant facial cues. Pediatrics, 122, 40–51.Google Scholar
Swain, J. E., Kim, P., Spicer, J., Ho, S. S., Dayton, C. J., Elmadih, A., & Abel, K. M. (2014). Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers. Brain Research, 1580, 78–101.Google Scholar
Talati, A., & Hirsch, J. (2005). Functional specialization within the medial frontal gyrus for perceptual go/no-go decisions based on “what,” “when,” and “where” related information: An fMRI study. Journal of Cognitive Neuroscience, 17, 981–993.Google Scholar
Teicher, M. H., Anderson, C. M., Ohashi, K., & Polcari, A. (2014). Childhood maltreatment: Altered network centrality of cingulate, precuneus, temporal pole and insula. Biological Psychiatry, 76, 297–305.Google Scholar
Tricomi, E. M., Delgado, M. R., & Fiez, J. A. (2004). Modulation of caudate activity by action contingency. Neuron, 41, 281–292.Google Scholar
Tricomi, E. M., Delgado, M. R., McCandliss, B. D., McClelland, J. L., & Fiez, J. A. (2006). Performance feedback drives caudate activation in a phonological learning task. Journal of Cognitive Neuroscience, 18, 1029–1043.CrossRefGoogle Scholar
van Veluw, S. J., & Chance, S. A. (2014). Differentiating between self and others: An ALE meta-analysis of fMRI studies of self-recognition and theory of mind. Brain Imaging and Behavior, 8, 24–38.Google Scholar
Warren, S. L., Bost, K. K., Roisman, G. I., Silton, R. L., Spielberg, J. M., Engels, A. S., … Heller, W. (2010). Effects of adult attachment and emotional distractors on brain mechanisms of cognitive control. Psychological Science, 21, 1818–1826.Google Scholar