Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-12-01T04:41:40.007Z Has data issue: false hasContentIssue false
  • English
  • Français

Parenting style moderates the effects of exposure to natural disaster-related stress on the neural development of reactivity to threat and reward in children

Published online by Cambridge University Press:  06 February 2019

Ellen M. Kessel ,
Brady D. Nelson ,
Megan Finsaas ,
Autumn Kujawa ,
Alexandria Meyer ,
Evelyn Bromet ,
Gabrielle A. Carlson ,
Greg Hajcak ,
Roman Kotov  and
Daniel N. Klein
Ellen M. Kessel*
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY, USA
Brady D. Nelson
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY, USA
Megan Finsaas
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY, USA
Autumn Kujawa
Affiliation:
Department of Psychology and Human Development, Vanderbilt University, Nashville, TN, USA
Alexandria Meyer
Affiliation:
Department of Psychology, Florida State University, Tallahassee, FL, USA
Evelyn Bromet
Affiliation:
Department of Psychiatry, Stony Brook University Medical Center, Stony Brook, NY, USA
Gabrielle A. Carlson
Affiliation:
Department of Psychiatry, Stony Brook University Medical Center, Stony Brook, NY, USA
Greg Hajcak
Affiliation:
Department of Psychology, Florida State University, Tallahassee, FL, USA
Roman Kotov
Affiliation:
Department of Psychiatry, Stony Brook University Medical Center, Stony Brook, NY, USA
Daniel N. Klein
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY, USA
*
Address for correspondence: Ellen M. Kessel, Department of Psychology, Stony Brook University, Stony Brook, NY 11794-2500. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Little is known about the effect of natural disasters on children's neural development. Additionally, despite evidence that stress and parenting may both influence the development of neural systems underlying reward and threat processing, few studies have brought together these areas of research. The current investigation examined the effect of parenting styles and hurricane-related stress on the development of neural reactivity to reward and threat in children. Approximately 8 months before and 9 months after Hurricane Sandy, 74 children experiencing high and low levels of hurricane-related stress completed tasks that elicited the reward positivity and error-related negativity, event-related potentials indexing sensitivity to reward and threat, respectively. At the post-Hurricane assessment, children completed a self-report questionnaire to measure promotion- and prevention-focused parenting styles. Among children exposed to high levels of hurricane-related stress, lower levels of promotion-focused, but not prevention-focused, parenting were associated with a reduced post-Sandy reward positivity. In addition, in children with high stress exposure, greater prevention-focused, but not promotion-focused, parenting was associated with a larger error-related negativity after Hurricane Sandy. These findings highlight the need to consider contextual variables such as parenting when examining how exposure to stress alters the development of neural reactivity to reward and threat in children.

Keywords

brain developmentevent-related potentialsnatural disasterparenting
Type
Regular Articles
Information
Development and Psychopathology , Volume 31 , Issue 4 , October 2019 , pp. 1589 - 1598
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Admon, R., Lubin, G., Stern, O., Rosenberg, K., Sela, L., Ben-Ami, H., & Hendler, T. (2009). Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity. Proceedings of the National Academy of Sciences of the United States of America, 106, 14120–14125.Google Scholar
Admon, R., Leykin, D., Lubin, G., Engert, V., Andrews, J., Pruessner, J., & Hendler, T. (2013). Stress-induced reduction in hippocampal volume and connectivity with the ventromedial prefrontal cortex are related to maladaptive responses to stressful military service. Human Brain Mapping, 34, 2808–2816.Google Scholar
Baskin-Sommers, A. R., & Foti, D. (2015). Abnormal reward functioning across substance use disorders and major depressive disorder: Considering reward as a transdiagnostic mechanism. International Journal of Psychophysiology, 98, 227–239.Google Scholar
Belsky, J. (2016). The differential susceptibility hypothesis: Sensitivity to the environment for better and for worse. JAMA Pediatrics, 170, 321–322.Google Scholar
Bernier, A., Calkins, S. D., & Bell, M. A. (2016). Longitudinal associations between the quality of mother–infant interactions and brain development across infancy. Child Development, 87, 1159–1174.Google Scholar
Blair, C., Raver, C., Granger, D., Mills-Koonce, R., Hibel, L., & Family Life Project Key Investigators. (2011). Allostasis and allostatic load in the context of poverty in early childhood. Development and Psychopathology, 23, 845.Google Scholar
Bowlby, J. (1973). Attachment and Loss. Vol. 2. Separation: Anxiety and Anger. New York, NY: Basic Books.Google Scholar
Brooker, R. J., & Buss, K. A. (2014). Harsh parenting and fearfulness in toddlerhood interact to predict amplitudes of preschool error-related negativity. Developmental Cognitive Neuroscience, 9, 148–159.Google Scholar
Bress, J. N., & Hajcak, G. (2013). Self-report and behavioral measures of reward sensitivity predict the feedback negativity. Psychophysiology, 50, 610–616.Google Scholar
Bress, J. N., Meyer, A., & Proudfit, G. H. (2015). The stability of the feedback negativity and its relationship with depression during childhood and adolescence. Development and Psychopathology, 27, 1285–1294.Google Scholar
Briggs-Gowan, M. J., Pollak, S. D., Grasso, D., Voss, J., Mian, N. D., Zobel, E., … & Pine, D. S. (2015). Attention bias and anxiety in young children exposed to family violence. Journal of Child Psychology and Psychiatry, 56, 1194–1201.Google Scholar
Casement, M., Guyer, A. E., Hipwell, A. E., McAloon, R. L., Hoffmann, A. M., Keenan, K. E., & Forbes, E. E. (2014). Girls’ challenging social experiences in early adolescence predict neural response to rewards and depressive symptoms. Developmental Cognitive Neuroscience, 8, 18–27.Google Scholar
Carlson, J. M., Cha, J., & Mujica-Parodi, L. R. (2013). Functional and structural amygdala–anterior cingulate connectivity correlates with attentional bias to masked fearful faces. Cortex, 49, 2595–2600.Google Scholar
Carlson, J. M., Foti, D., Mujica-Parodi, L. R., Harmon-Jones, E., & Hajcak, G. (2011). Ventral striatal and medial prefrontal BOLD activation is correlated with reward-related electrocortical activity: A combined ERP and fMRI study. Neuroimage, 57, 1608–1616.Google Scholar
Carter, C. S., & van Veen, V. (2007). Anterior cingulate cortex and conflict detection: An update of theory and data. Cognitive Affective & Behavioral Neuroscience, 7, 367–379.Google Scholar
Costa, N. M., Weems, C. F., & Pina, A. A. (2009). Hurricane Katrina and youth anxiety: The role of perceived attachment beliefs and parenting behaviors. Journal of Anxiety Disorders, 23, 935–941.Google Scholar
DeGarmo, D. S., Patterson, G. R., & Forgatch, M. S. (2004). How do outcomes in a specified parent training intervention maintain or wane over time? Prevention Science, 5(2), 73–89.Google Scholar
DelGiudice, M. (2014). Middle childhood: An evolutionary-developmental synthesis. Child Development Perspectives, 8, 193–200.Google Scholar
Energy Climate Intelligence Unit. (2017). Heavy Weather: Tracking the Fingerprints of Climate Change, Two Years After the Paris Summit. Retrieved from https://eciu.net/assets/Reports/ECIU_Climate_Attribution-report-Dec-2017.pdfGoogle Scholar
Eriksen, B. A., & Eriksen, C. W. (1974). Effects of noise letters upon the identification of a target letter in a nonsearch task. Perception & Psychophysics, 16(1), 143–149.Google Scholar
Euser, A. S., Evans, B. E., Greaves-Lord, K., Huizink, A. C., & Franken, I. H. (2013). Parental rearing behavior prospectively predicts adolescents’ risky decision-making and feedback-related electrical brain activity. Developmental Science, 16, 409–427.Google Scholar
Foti, D., & Hajcak, G. (2009). Depression and reduced sensitivity to non-rewards versus rewards: Evidence from event-related potentials. Biological Psychology, 81(1), 1–8.Google Scholar
Gard, A. M., Waller, R., Shaw, D. S., Forbes, E. E., Hariri, A. R., & Hyde, L. W. (2017). The long reach of early adversity: Parenting, stress, and neural pathways to antisocial behavior in adulthood. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2, 582–590.Google Scholar
Galea, S., Brewin, C. R., Gruber, M., Jones, R. T., King, D. W., King, L. A., … Kessler, R. C. (2007). Exposure to hurricane-related stressors and mental illness after Hurricane Katrina. Archives of General Psychiatry, 64, 1427–1434.Google Scholar
Gehring, W. J., & Fencsik, D. E. (2001). Functions of the medial frontal cortex in the processing of conflict and errors. The Journal of Neuroscience, 21, 9430–9437.Google Scholar
Gehring, W. J., & Willoughby, A. R. (2002). The medial frontal cortex and the rapid processing of monetary gains and losses. Science, 295, 2279–2282.Google Scholar
Goff, B., Gee, D. G., Telzer, E. H., Humphreys, K. L., Gabard-Durnam, L., Flannery, J., & Tottenham, N. (2013). Reduced nucleus accumbens reactivity and adolescent depression following early-life stress. Neuroscience, 249, 129–138.Google Scholar
Gollier-Briant, F., Paillère-Martinot, M. L., Lemaitre, H., Miranda, R., Vulser, H., Goodman, R., … & Poustka, L. (2016). Neural correlates of three types of negative life events during angry face processing in adolescents. Social Cognitive and Affective Neuroscience, 11, 1961–1969.Google Scholar
Gratton, G., Coles, M. G., & Donchin, E. (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology, 55(4), 468–484.Google Scholar
Hajcak, G. (2012). What we've learned from mistakes: Insights from error-related brain activity. Current Directions in Psychological Science, 21, 101–106.Google Scholar
Hanson, J. L., Albert, D., Iselin, A. M. R., Carré, J. M., Dodge, K. A., & Hariri, A. R. (2015). Cumulative stress in childhood is associated with blunted reward-related brain activity in adulthood. Social Cognitive and Affective Neuroscience, 11, 405–412.Google Scholar
Holroyd, C. B., & Coles, M. G. (2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review, 109, 679.Google Scholar
Higgins, E. T. (1997). Beyond pleasure and pain. American Psychologist, 52, 1280.Google Scholar
Higgins, E. T. (2001). Promotion and prevention experiences: Relating emotions to nonemotional motivational states. In Forgas, J. P. (Ed.), Handbook of Affect and Social Cognition (pp. 186–211). Hillsdale, NJ: Lawrence Erlbaum Associates.Google Scholar
Hudson, J. L., & Rapee, R. M. (2004). From anxious temperament to disorder: an etiological model. In Heimberg, R. G., Turk, C. L., & Mennin, D. S. (Eds.), Generalized Anxiety Disorder: Advances in Research and Practice (pp. 51–74). New York: The Guilford Press.Google Scholar
Inzlicht, M., Bartholow, B.D., & Hirsch, J.B. (2015). Emotional foundations of cognitive control. Trends in Cognitive Sciences, 19, 126–132.Google Scholar
Jackson, F., Nelson, B. D., & Proudfit, G. H. (2015). In an uncertain world, errors are more aversive: Evidence from the error-related negativity. Emotion, 15, 12.Google Scholar
Kessel, E. M., Huselid, R. F., DeCicco, J. M., & Dennis, T. A. (2013). Neurophysiological processing of emotion and parenting interact to predict inhibited behavior: An affective-motivational framework. Frontiers in Human Neuroscience, 7, 326.Google Scholar
Kopala-Sibley, D. C., Kotov, R., Bromet, E. J., Carlson, G. A., Danzig, A. P., Black, S. R., & Klein, D. N. (2016). Personality diatheses and Hurricane Sandy: effects on post-disaster depression. Psychological Medicine, 46, 865–875.Google Scholar
Levinson, A. R., Speed, B. C., Infantolino, Z. P., & Hajcak, G. (2017). Reliability of the electrocortical response to gains and losses in the doors task. Psychophysiology, 54, 601–607.Google Scholar
Luby, J., Belden, A., Botteron, K., Marrus, N., Harms, M. P., Babb, C., … & Barch, D. (2013). The effects of poverty on childhood brain development: The mediating effect of caregiving and stressful life events. JAMA Pediatrics, 167, 1135–1142.Google Scholar
Maclean, J. C., Popovici, I., & French, M. T. (2016). Are natural disasters in early childhood associated with mental health and substance use disorders as an adult? Social Science & Medicine, 151, 78–91.Google Scholar
Masten, A. S. (2001). Ordinary magic: Resilience processes in development. American Psychologist, 56, 227.Google Scholar
Masten, A. S., & Cicchetti, D. (2010). Developmental cascades. Development and Psychopathology, 22, 491–495.Google Scholar
Masten, A. S., & Narayan, A. J. (2012). Child development in the context of disaster, war, and terrorism: Pathways of risk and resilience. Annual Review of Psychology, 63, 227–257.Google Scholar
McCrory, E. J., Gerin, M. I., & Viding, E. (2017). Annual research review: Childhood maltreatment, latent vulnerability and the shift to preventative psychiatry – the contribution of functional brain imaging. Journal of Child Psychology and Psychiatry, 58, 338–357. doi:10.1111/jcpp.12713Google Scholar
Meyer, A., Bress, J. N., & Proudfit, G. H. (2014). Psychometric properties of the error-related negativity in children and adolescents. Psychophysiology, 51, 602–610.Google Scholar
Meyer, A., Proudfit, G. H., Bufferd, S. J., Kujawa, A. J., Laptook, R. S., Torpey, D. C., & Klein, D. N. (2015). Self-reported and observed punitive parenting prospectively predicts increased error-related brain activity in six-year-old children. Journal of Abnormal Child Psychology, 43, 821–829.Google Scholar
Meyer, A., Danielson, C. K., Danzig, A. P., Bhatia, V., Black, S. R., Bromet, E., … & Klein, D. N. (2017). Neural biomarker and early temperament predict increased internalizing symptoms after a natural disaster. Journal of the American Academy of Child & Adolescent Psychiatry, 56, 410–416.Google Scholar
Milevsky, A., Schlechter, M., Netter, S., & Keehn, D. (2007). Maternal and paternal parenting styles in adolescents: Associations with self-esteem, depression and life-satisfaction. Journal of Child and Family Studies, 16, 39–47.Google Scholar
Nelson, B. D., Kessel, E. M., Jackson, F., & Hajcak, G. (2016). The impact of an unpredictable context and intolerance of uncertainty on the electrocortical response to monetary gains and losses. Cognitive Affective & Behavioral Neuroscience, 16, 153–163.Google Scholar
Nelson, B. D., Perlman, G., Klein, D. N., Kotov, R., & Hajcak, G. (2016). Blunted neural response to rewards as a prospective predictor of the development of depression in adolescent girls. American Journal of Psychiatry, 173, 1223–1230.Google Scholar
Neria, Y., & Shultz, J. M. (2012). Mental health effects of Hurricane Sandy: Characteristics, potential aftermath, and response. Journal of the American Medical Association, 308, 2571–2572.Google Scholar
Norris, F. H., Sherrieb, K., & Galea, S. (2010). Prevalence and consequences of disaster-related illness and injury from Hurricane Ike. Rehabilitation Psychology, 55, 221–230.Google Scholar
Olino, T. M., Klein, D. N., Dyson, M. W., Rose, S. A., & Durbin, C. E. (2010). Temperamental emotionality in preschool-aged children and depressive disorders in parents: Associations in a large community sample. Journal of Abnormal Psychology 119, 468–478.Google Scholar
Proudfit, G. H., Inzlicht, M., & Mennin, D. S. (2013). Anxiety and error monitoring: The importance of motivation and emotion. Frontiers in Human Neuroscience, 7.Google Scholar
Ridderinkhof, K. R., Van Den Wildenberg, W. P., Segalowitz, S. J., & Carter, C. S. (2004). Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain and Cognition, 56(2), 129–14.Google Scholar
Riesel, A., Weinberg, A., Endrass, T., Kathmann, N., & Hajcak, G. (2012). Punishment has a lasting impact on error-related brain activity. Psychophysiology, 49, 239–247.Google Scholar
Spell, A. W., Kelley, M. L., Wang, J., Self-Brown, S., Davidson, K. L., Pellegrin, A., … & Baumeister, A. (2008). The moderating effects of maternal psychopathology on children's adjustment post -hurricane Katrina. Journal of Clinical Child & Adolescent Psychology, 37(3), 553–563.Google Scholar
Strauman, T. J. (2006). Adolescent Regulatory Focus Questionnaire. Unpublished questionnaire, Duke University, Durham, NC.Google Scholar
Swartz, J. R., Williamson, D. E., & Hariri, A. R. (2015). Developmental change in amygdala reactivity during adolescence: Effects of family history of depression and stressful life events. American Journal of Psychiatry, 172, 276–283.Google Scholar
Taylor, S. F., Stern, E. R., & Gehring, W. J. (2007). Neural systems for error monitoring: Recent findings and theoretical perspectives. Neuroscientist, 13, 160–172.Google Scholar
Weems, C. F. (2015). Biological correlates of child and adolescent responses to disaster exposure: A bio-ecological model. Current Psychiatry Reports, 17, 51.Google Scholar
Weinberg, A., Riesel, A., & Hajcak, G. (2012). Integrating multiple perspectives on error-related brain activity: The ERN as a neural indicator of trait defensive reactivity. Motivation and Emotion, 36, 84–100.Google Scholar
Whittle, S., Vijayakumar, N., Simmons, J. G., Dennison, M., Schwartz, O., Pantelis, C., … & Allen, N. B. (2017). Role of positive parenting in the association between neighborhood social disadvantage and brain development across adolescence. JAMA Psychiatry, 74, 824–832.Google Scholar