Skip to main content Accessibility help

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

  • Karina Quevedo (a1), Theodore E. A. Waters (a2), Hannah Scott (a1), Glenn I. Roisman (a1), Daniel S. Shaw (a3) and Erika E. Forbes (a3)...


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.


Corresponding author

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:


Hide All

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.



Hide All
Ainsworth, M. S., Blehar, M. C., Waters, E., & Wall, S. (1978). Patterns of attachment: A psychological study of the strange situation. Oxford: Erlbaum.
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, 233243.
Balleine, B. W., & Killcross, S. (2006). Parallel incentive processing: An integrated view of amygdala function. Trends in Neuroscience, 29, 272279.
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, 18521865.
Bowlby, J. (1980). Attachment and loss. New York: Basic Books. (Original work published 1969)
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, 523528.
Cassidy, J. (1994). Emotion regulation: Influences of attachment relationships. Monographs of the Society for Research in Child Development, 59(2–3), 228249.
Cassidy, J., & Shaver, P. R. (Eds.). (2008). Handbook of attachment: Theory, research, and clinical applications (2nd ed.). New York: Guilford Press.
Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129(Pt. 3), 564583.
Cunningham, W. A., Brosch, T. (2012). Motivational salience amygdala tuning from traits, needs, values, and goals. Current Directions in Psychological Science, 21, 5459.
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, 30723077.
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, 596603.
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, 435456.
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, 6473.
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, 1125.
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, 633639.
Gander, M., & Buchheim, A. (2015). Attachment classification, psychophysiology and frontal EEG asymmetry across the lifespan: A review. Frontiers of Human Neuroscience, 9, 79.
Goel, V., & Dolan, R. J. (2001). Functional neuroanatomy of three-term relational reasoning. Neuropsychologia, 39, 901909.
Grahn, J. A., Parkinson, J. A., & Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Progress in Neurobiology, 86, 141155.
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, 103136.
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.
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, 591610.
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, 25642570.
Kobayakawa, M., & Kawamura, M. (2011). Neural and cognitive correlates of social cognition: Findings on neuropsychological and neuroimaging studies. Brain Nerve, 63, 13521360.
Koechlin, E., & Hyafil, A. (2007). Anterior prefrontal function and the limits of human decision-making. Science, 318, 594598.
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, 623635.
Luking, K. R., & Barch, D. M. (2013). Candy and the brain: Neural response to candy gains and losses. Cognitive Affective & Behavioral Neuroscience, 13, 437451.
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, 18351838.
Madigan, S., Atkinson, L., Laurin, K., & Benoit, D. (2013). Attachment and internalizing behavior in early childhood: A meta-analysis. Developmental Psychology, 49, 672689.
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.
McGaugh, J. L. (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience, 27, 128.
Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: A network model of insula function. Brain Structure and Function, 214, 655667.
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. 503531). New York: Guilford Press.
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, 77102.
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 167202.
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, 108117.
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, 9991008.
Murray, L. (1992). The impact of postnatal depression on infant development. Journal of Child Psychology and Psychiatry, 33, 543561.
Packard, M. G., & Knowlton, B. J. (2002). Learning and memory functions of the basal ganglia. Annual Review of Neuroscience, 25, 563593.
Petrides, M. (2005). Lateral prefrontal cortex: Architectonic and functional organization. Philosophical Transactions of the Royal Society of London B, 360, 781795.
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, 289304.
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, 533551.
Shaw, D. S., Gilliom, M., Ingoldsby, E. M., & Nagin, D. S. (2003). Trajectories leading to school-age conduct problems. Developmental Psychology, 39, 189200.
Strathearn, L., Fonagy, P., Amico, J., & Montague, P. R. (2009). Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology, 34, 26552666.
Strathearn, L., Li, J., Fonagy, P., & Montague, P. R. (2008). What's in a smile? Maternal brain responses to infant facial cues. Pediatrics, 122, 4051.
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, 78101.
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, 981993.
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, 297305.
Tricomi, E. M., Delgado, M. R., & Fiez, J. A. (2004). Modulation of caudate activity by action contingency. Neuron, 41, 281292.
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, 10291043.
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, 2438.
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, 18181826.

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

  • Karina Quevedo (a1), Theodore E. A. Waters (a2), Hannah Scott (a1), Glenn I. Roisman (a1), Daniel S. Shaw (a3) and Erika E. Forbes (a3)...


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed