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

Published online by Cambridge University Press:  12 April 2017

James E. Swain*
Affiliation:
Stony Brook University Medical Center University of Michigan, Ann Arbor Yale University
S. Shaun Ho
Affiliation:
Stony Brook University Medical Center
Katherine L. Rosenblum
Affiliation:
University of Michigan, Ann Arbor
Diana Morelen
Affiliation:
East Tennessee State University
Carolyn J. Dayton
Affiliation:
Wayne State University
Maria Muzik
Affiliation:
University of Michigan, Ann Arbor
*
Address correspondence and reprint requests to: James E. Swain, Department of Psychiatry, Stony Brook University Medical Center, HSC, T10-020, Stony Brook, NY 11794-8101; E-mail: james.swain@stonybrookmedicine.edu.

Abstract

Parental responses to their children are crucially influenced by stress. However, brain-based mechanistic understanding of the adverse effects of parenting stress and benefits of therapeutic interventions is lacking. We studied maternal brain responses to salient child signals as a function of Mom Power (MP), an attachment-based parenting intervention established to decrease maternal distress. Twenty-nine mothers underwent two functional magnetic resonance imaging brain scans during a baby-cry task designed to solicit maternal responses to child's or self's distress signals. Between scans, mothers were pseudorandomly assigned to either MP (n = 14) or control (n = 15) with groups balanced for depression. Compared to control, MP decreased parenting stress and increased child-focused responses in social brain areas highlighted by the precuneus and its functional connectivity with subgenual anterior cingulate cortex, which are key components of reflective self-awareness and decision-making neurocircuitry. Furthermore, over 13 weeks, reduction in parenting stress was related to increasing child- versus self-focused baby-cry responses in amygdala–temporal pole functional connectivity, which may mediate maternal ability to take her child's perspective. Although replication in larger samples is needed, the results of this first parental-brain intervention study demonstrate robust stress-related brain circuits for maternal care that can be modulated by psychotherapy.

Type
Special Issue Articles
Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

This article is supported by the Brain and Behavior Research Foundation (to J.E.S.), the State of Michigan, Department of Community Health (2009–2010, to M.M.); the University of Michigan's Injury Center (Center for Disease Control and Prevention U49/CE002099); the Center for Human Growth and Development (to J.E.S.); the Robert Wood Johnson Foundation Health and Society Scholar Awards (to J.E.S. and M.M.); and the National Institutes for Health National Center for Advanced Translational Sciences via the Michigan Institute for Clinical Health Research UL1TR000433 (to J.E.S., S.S.H., C.J.D., K.L.R., and M.M.).

References

Abidin, R. (1995). Parenting Stress Index. Lutz, FL: Psychological Assessment Resources.Google Scholar
Ainsworth, M. D., & Bell, S. M. (1970). Attachment, exploration, and separation: Illustrated by the behavior of one-year-olds in a strange situation. Child Development, 41, 4967.CrossRefGoogle Scholar
Atzil, S., Hendler, T., & Feldman, R. (2011). Specifying the neurobiological basis of human attachment: Brain, hormones, and behavior in synchronous and intrusive mothers. Neuropsychopharmacology, 36, 26032615. doi:10.1038/npp.2011.172 CrossRefGoogle ScholarPubMed
Atzil, S., Hendler, T., Zagoory-Sharon, O., Winetraub, Y., & Feldman, R. (2012). Synchrony and specificity in the maternal and the paternal brain: Relations to oxytocin and vasopressin. Journal of the American Academy of Child & Adolescent Psychiatry, 51, 798811. doi:10.1016/j.jaac.2012.06.008 CrossRefGoogle ScholarPubMed
Ball, T., Rahm, B., Eickhoff, S. B., Schulze-Bonhage, A., Speck, O., & Mutschler, I. (2007). Response properties of human amygdala subregions: Evidence based on functional MRI combined with probabilistic anatomical maps. PLOS ONE, 2, e307. doi:10.1371/journal.pone.0000307 CrossRefGoogle ScholarPubMed
Barrett, J., & Fleming, A. S. (2011). Annual Research Review: All mothers are not created equal: Neural and psychobiological perspectives on mothering and the importance of individual differences. Journal of Child Psychology and Psychiatry, 52, 368397.CrossRefGoogle Scholar
Barrett, J., Wonch, K. E., Gonzalez, A., Ali, N., Steiner, M., Hall, G. B., & Fleming, A. S. (2012). Maternal affect and quality of parenting experiences are related to amygdala response to infant faces. Social Neuroscience, 7, 252268. doi:10.1080/17470919.2011.609907 CrossRefGoogle ScholarPubMed
Beck, C. T., & Gable, R. K. (2001). Further validation of the Postpartum Depression Screening Scale. Nursing Research, 50, 155164.CrossRefGoogle ScholarPubMed
Bowlby, J. (1958). The nature of the child's tie to his mother. International Journal of Psychoanalysis, 39, 350373.Google ScholarPubMed
Bowlby, J. (1978). Attachment theory and its therapeutic implications. Adolescent Psychiatry, 6, 533.Google ScholarPubMed
Cardinal, R. N., Parkinson, J. A., Hall, J., & Everitt, B. J. (2002). Emotion and motivation: The role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience & Biobehavioral Reviews, 26, 321352.CrossRefGoogle ScholarPubMed
Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3, 201215. doi:10.1038/nrn755 CrossRefGoogle ScholarPubMed
Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162173.CrossRefGoogle ScholarPubMed
CSSP. (2015). Strengthening Families™: A Protective Factors Framework. Retrieved from http://www.cssp.org/reform/strengtheningfamilies Google Scholar
Dayton, C. J., Huth-Bocks, A. C., & Busuito, A. (2016). The influence of interpersonal aggression on maternal perceptions of infant emotions: Associations with early parenting quality. Emotion, 16, 436448. doi:10.1037/emo0000114 CrossRefGoogle ScholarPubMed
Decety, J., & Lamm, C. (2007). The role of the right temporoparietal junction in social interaction: How low-level computational processes contribute to meta-cognition. Neuroscientist, 13, 580593.CrossRefGoogle ScholarPubMed
De Pisapia, N., Bornstein, M. H., Rigo, P., Esposito, G., De Falco, S., & Venuti, P. (2013). Sex differences in directional brain responses to infant hunger cries. NeuroReport, 24, 142146. doi:10.1097/WNR.0b013e32835df4fa CrossRefGoogle ScholarPubMed
Etkin, A., Prater, K. E., Schatzberg, A. F., Menon, V., & Greicius, M. D. (2009). Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Archives of General Psychiatry, 66, 13611372. doi:66/12/1361[pii]10.1001/archgenpsychiatry.2009.104 CrossRefGoogle ScholarPubMed
Feldman, R., & Eidelman, A. I. (2009). Biological and environmental initial conditions shape the trajectories of cognitive and social-emotional development across the first years of life. Developmental Science, 12, 194200.CrossRefGoogle ScholarPubMed
Feldman, R., Granat, A., Pariente, C., Kanety, H., Kuint, J., & Gilboa-Schechtman, E. (2009). Maternal depression and anxiety across the postpartum year and infant social engagement, fear regulation, and stress reactivity. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 919927.CrossRefGoogle ScholarPubMed
Goldberg, I. I., Harel, M., & Malach, R. (2006). When the brain loses its self: Prefrontal inactivation during sensorimotor processing. Neuron, 50, 329339. doi:10.1016/j.neuron.2006.03.015 CrossRefGoogle ScholarPubMed
Haggard, P. (2008). Human volition: Towards a neuroscience of will. Nature Reviews Neuroscience, 9, 934946.CrossRefGoogle ScholarPubMed
Hipwell, A. E., Guo, C., Phillips, M. L., Swain, J. E., & Moses-Kolko, E. L. (2015). Right frontoinsular cortex and subcortical activity to infant cry is associated with maternal mental state talk. Journal of Neuroscience, 35, 1272512732. doi:10.1523/jneurosci.1286-15.2015 CrossRefGoogle ScholarPubMed
Ho, S. S., Konrath, S., Brown, S., & Swain, J. E. (2014). Empathy and stress related neural responses in maternal decision making. Frontiers in Neuroscience, 8, 152. doi:10.3389/fnins.2014.00152 CrossRefGoogle ScholarPubMed
Kim, P., Feldman, R., Mayes, L. C., Eicher, V., Thompson, N., Leckman, J. F., & Swain, J. E. (2011). Breastfeeding, brain activation to own infant cry, and maternal sensitivity. Journal of Child Psychology and Psychiatry, 52, 907915.CrossRefGoogle ScholarPubMed
Kim, P., Ho, S. S., Evans, G. W., Liberzon, I., & Swain, J. E. (2015). Childhood social inequalities influences neural processes in young adult caregiving. Development and Psychobiology, 57, 948960. doi:10.1002/dev.21325 CrossRefGoogle ScholarPubMed
Kim, P., Leckman, J. F., Mayes, L. C., Feldman, R., Wang, X., & Swain, J. E. (2010). The plasticity of human maternal brain: Longitudinal changes in brain anatomy during the early postpartum period. Behavioral Neuroscience, 124, 695700.CrossRefGoogle ScholarPubMed
Kim, P., Leckman, J. F., Mayes, L. C., Newman, M. A., Feldman, R., & Swain, J. E. (2010). Perceived quality of maternal care in childhood and structure and function of mothers’ brain. Developmental Science, 13, 662673. doi:10.1111/j.1467-7687.2009.00923.x CrossRefGoogle ScholarPubMed
Kim, P., Mayes, L., Feldman, R., Leckman, J. F., & Swain, J. E. (2013). Early postpartum parental preoccupation and positive parenting thoughts: Relationship with parent–infant interaction. Infant Mental Health Journal, 34, 104116. doi:10.1002/Imhj.21359 CrossRefGoogle ScholarPubMed
Kim, P., Rigo, P., Leckman, J. F., Mayes, L. C., Cole, P. M., Feldman, R., & Swain, J. E. (2015). A prospective longitudinal study of perceived infant outcomes at 18–24 months: Neural and psychological correlates of parental thoughts and actions assessed during the first month postpartum. Frontiers in Psychology, 6, 1772. doi:10.3389/fpsyg.2015.01772 CrossRefGoogle ScholarPubMed
Kim, P., Rigo, P., Mayes, L. C., Feldman, R., Leckman, J. F., & Swain, J. E. (2014). Neural plasticity in fathers of human infants. Social Neuroscience, 9, 522535. doi:10.1080/17470919.2014.933713 CrossRefGoogle ScholarPubMed
Kim, P., Strathearn, L., & Swain, J. E. (2016). The maternal brain and its plasticity in humans. Hormones and Behavior, 77, 113123. doi:10.1016/j.yhbeh.2015.08.001 CrossRefGoogle ScholarPubMed
Kim, S., Fonagy, P., Allen, J., & Strathearn, L. (2014). Mothers’ unresolved trauma blunts amygdala response to infant distress. Social Neuroscience, 9, 352363. doi:10.1080/17470919.2014.896287 CrossRefGoogle ScholarPubMed
Laurent, H. K., & Ablow, J. C. (2012a). A cry in the dark: Depressed mothers show reduced neural activation to their own infant's cry. Social Cognitive & Affective Neuroscience, 7, 125134. doi:10.1093/scan/nsq091 CrossRefGoogle ScholarPubMed
Laurent, H. K., & Ablow, J. C. (2012b). The missing link: Mothers’ neural response to infant cry related to infant attachment behaviors. Infant Behavior and Development, 35, 761772. doi:10.1016/j.infbeh.2012.07.007 CrossRefGoogle ScholarPubMed
LeDoux, J. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155184. doi:10.1146/annurev.neuro.23.1.155 CrossRefGoogle ScholarPubMed
LeDoux, J. (2012). Rethinking the emotional brain. Neuron, 73, 653676. http://dx.doi.org/10.1016/j.neuron.2012.02.004 CrossRefGoogle ScholarPubMed
Lenzi, D., Trentini, C., Pantano, P., Macaluso, E., Iacoboni, M., Lenzi, G. L., & Ammaniti, M. (2009). Neural basis of maternal communication and emotional expression processing during infant preverbal stage. Cerebral Cortex, 19, 11241133.CrossRefGoogle ScholarPubMed
McLaren, D. G., Ries, M. L., Xu, G., & Johnson, S. C. (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches. NeuroImage, 61, 12771286. doi:10.1016/j.neuroimage.2012.03.068 CrossRefGoogle ScholarPubMed
Moses-Kolko, E. L., Horner, M. S., Phillips, M. L., Hipwell, A. E., & Swain, J. E. (2014). In search of neural endophenotypes of postpartum psychopathology and disrupted maternal caregiving. Journal of Neuroendocrinology, 26, 665684. doi:10.1111/jne.12183 CrossRefGoogle ScholarPubMed
Moses-Kolko, E. L., Perlman, S. B., Wisner, K. L., James, J., Saul, A. T., & Phillips, M. L. (2010). Abnormally reduced dorsomedial prefrontal cortical activity and effective connectivity with amygdala in response to negative emotional faces in postpartum depression. American Journal of Psychiatry, 167, 13731380.CrossRefGoogle ScholarPubMed
Muzik, M., Rosenblum, K. L., Alfafara, E. A., Schuster, M. M., Miller, N. M., Waddell, R. M., & Kohler, E. S. (2015). Mom Power: Preliminary outcomes of a group intervention to improve mental health and parenting among high-risk mothers. Archives of Women's Mental Health. Advance online publication. doi:10.1007/s00737-014-0490-z CrossRefGoogle ScholarPubMed
Muzik, M., Rosenblum, K. L., & Schuster, M. M. (2010). Mom Power 10 Week Curriculum. Unpublished manuscript, University of Michigan, Department of Psychiatry.Google Scholar
Muzik, M., Rosenblum, K. L., Schuster, M. M., Kohler, E. S., Alfafara, E. A., & Miller, N. M. (2016). A mental health and parenting intervention for adolescent and young adult mothers and their infants. Journal of Depression and Anxiety, 5, 233239. doi:10.4172/2167-1044.1000233 Google Scholar
Otti, A., Guendel, H., Laer, L., Wohlschlaeger, A. M., Lane, R. D., Decety, J., … Noll-Hussong, M. (2010). I know the pain you feel—How the human brain's default mode predicts our resonance to another's suffering. Neuroscience, 169, 143148. doi:10.1016/j.neuroscience.2010.04.072 CrossRefGoogle ScholarPubMed
Pizzagalli, D. A. (2014). Depression, stress, and anhedonia: Toward a synthesis and integrated model. Annual Review of Clinical Psychology, 10, 393423. doi:10.1146/annurev-clinpsy-050212-185606 CrossRefGoogle Scholar
Pohlack, S. T., Nees, F., Ruttorf, M., Schad, L. R., & Flor, H. (2012). Activation of the ventral striatum during aversive contextual conditioning in humans. Biological Psychology, 91, 7480. doi:10.1016/j.biopsycho.2012.04.004 CrossRefGoogle ScholarPubMed
Reitman, D., Currier, R. O., & Stickle, T. R. (2002). A critical evaluation of the Parenting Stress Index—Short Form (PSI-SF) in a Head Start Population. Journal of Clinical Child and Adolescent Psychology, 31, 384392. doi:10.1207/S15374424JCCP3103_10 CrossRefGoogle Scholar
Riem, M. M. E., Bakermans-Kranenburg, M. J., van IJzendoorn, M. H., Out, D., & Rombouts, S. (2012). Attachment in the brain: Adult attachment representations predict amygdala and behavioral responses to infant crying. Attachment & Human Development, 14, 533551. doi:10.1080/14616734.2012.727252 CrossRefGoogle ScholarPubMed
Sadaghiani, S., & D'Esposito, M. (2015). Functional characterization of the cingulo-opercular network in the maintenance of tonic Aaertness. Cerebral Cortex, 25, 27632773. doi:10.1093/cercor/bhu072 CrossRefGoogle Scholar
Schuster, M. (2013). Mom Power Fidelity Scale. Unpublished manuscript.Google Scholar
Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., … Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience, 27, 23492356. doi:10.1523/jneurosci.5587-06.2007 CrossRefGoogle ScholarPubMed
Silverman, M. E., Loudon, H., Safier, M., Protopopescu, X., Leiter, G., Liu, X., & Goldstein, M. (2007). Neural dysfunction in postpartum depression: An fMRI pilot study. CNS Spectrums, 12, 853862.CrossRefGoogle ScholarPubMed
Sripada, R. K., Swain, J. E., Evans, G. W., Welsh, R. C., & Liberzon, I. (2014). Childhood poverty and stress reactivity are associated with aberrant functional connectivity in default mode network. Neuropsychopharmacology, 39, 22442251. doi:10.1038/npp.2014.75 CrossRefGoogle ScholarPubMed
Strathearn, L., Fonagy, P., Amico, J., & Montague, P. R. (2009). Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropsychopharmacology, 34, 26552666.CrossRefGoogle ScholarPubMed
Strathearn, L., & Kim, S. (2013). Mothers’ amygdala response to positive or negative infant affect is modulated by personal relevance. Frontiers in Neuroscience, 7, 110. doi:10.3389/fnins.2013.00176 CrossRefGoogle ScholarPubMed
Swain, J. E. (2011). The human parental brain: In vivo neuroimaging. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 35, 12421254.CrossRefGoogle ScholarPubMed
Swain, J. E., Dayton, C. J., Kim, P., Tolman, R. M., & Volling, B. L. (2014). Progress on the paternal brain: Theory, animal models, human brain research, and mental health implications. Infant Mental Health Journal, 35, 394408. doi:10.1002/imhj.21471 CrossRefGoogle ScholarPubMed
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. doi:10.1016/j.brainres.2014.03.007 CrossRefGoogle ScholarPubMed
Swain, J. E., & Lorberbaum, J. P. (2008). Imaging the human parental brain. Neurobiology of the Parental Brain, 6, 83100. doi:10.1016/B978-0-12-374285-8.00006-8 CrossRefGoogle Scholar
Swain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007). Brain basis of early parent-infant interactions: Psychology, physiology, and in vivo functional neuroimaging studies. Journal of Child Psychology and Psychiatry, 48, 262287.CrossRefGoogle ScholarPubMed
Swain, J. E., Mayes, L. C., & Leckman, J. F. (2004). The development of parent-infant attachment through dynamic and interactive signaling loops of care and cry. Behavioral and Brain Sciences, 27, 472473.CrossRefGoogle Scholar
Swain, J. E., Tasgin, E., Mayes, L. C., Feldman, R., Constable, R. T., & Leckman, J. F. (2008). Maternal brain response to own baby-cry is affected by cesarean section delivery. Journal of Child Psychology and Psychiatry, 49, 10421052.CrossRefGoogle ScholarPubMed
Todorov, A., & Olson, I. R. (2008). Robust learning of affective trait associations with faces when the hippocampus is damaged, but not when the amygdala and temporal pole are damaged. Social Cognitive & Affective Neuroscience, 3, 195203. doi:10.1093/scan/nsn013 CrossRefGoogle Scholar
Venuti, P., Caria, A., Esposito, G., De Pisapia, N., Bornstein, M. H., & de Falco, S. (2012). Differential brain responses to cries of infants with autistic disorder and typical development: An fMRI study. Research in Developmental Disabilities, 33, 22552264. doi:10.1016/j.ridd.2012.06.011 CrossRefGoogle ScholarPubMed
Wan, M. W., Downey, D., Strachan, H., Elliott, R., Williams, S. R., & Abel, K. M. (2014). The neural basis of maternal bonding. PLOS ONE, 9, e88436. doi:10.1371/journal.pone.0088436 CrossRefGoogle ScholarPubMed
Whitfield-Gabrieli, S., & Ford, J. M. (2012). Default mode network activity and connectivity in psychopathology. Annual Review of Clinical Psychology, 8, 4976. doi:10.1146/annurev-clinpsy-032511-143049 CrossRefGoogle ScholarPubMed
Wonch, K. E., de Medeiros, C. B., Barrett, J. A., Dudin, A., Cunningham, W. A., Hall, G. B., … Fleming, A. S. (2016). Postpartum depression and brain response to infants: Differential amygdala response and connectivity. Social Neuroscience. Advance online publication. doi:10.1080/17470919.2015.1131193 CrossRefGoogle ScholarPubMed
Yaseen, Z. S., Zhang, X., Muran, J. C., Winston, A., & Galynker, I. I. (2016). Comparison of brain activity correlating with self-report versus narrative attachment measures during conscious appraisal of an attachment figure. Frontiers in Human Neuroscience, 10, 90. doi:10.3389/fnhum.2016.00090 CrossRefGoogle ScholarPubMed
Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., … Buckner, R. L. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106, 11251165. doi:10.1152/jn.00338.2011 Google ScholarPubMed