Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-06T11:00:38.825Z Has data issue: false hasContentIssue false

Emotion regulation in children with behavior problems: Linking behavioral and brain processes

Published online by Cambridge University Press:  11 July 2012

Isabela Granic*
Affiliation:
Radboud University Nijmegen
Liesel-Ann Meusel
Affiliation:
Rotman Research Institute
Connie Lamm
Affiliation:
University of New Orleans
Steven Woltering
Affiliation:
University of Toronto
Marc D. Lewis
Affiliation:
Radboud University Nijmegen
*
Address correspondence and reprint requests to: Isabela Granic, Department of Developmental Psychopathology, Radboud University Nijmegen, Behavioural Science Institute, Montessorilaan 3, Nijmegen 6525 HR, The Netherlands; E-mail: [email protected].

Abstract

Past studies have shown that aggressive children exhibit rigid (rather than flexible) parent–child interactions; these rigid repertoires may provide the context through which children fail to acquire emotion-regulation skills. Difficulties in regulating emotion are associated with minimal activity in dorsal systems in the cerebral cortex, for example, the anterior cingulate cortex. The current study aimed to integrate parent–child and neurocognitive indices of emotion regulation and examine their associations for the first time. Sixty children (8–12 years old) referred for treatment for aggression underwent two assessments. Brain processes related to emotion regulation were assessed using dense-array EEG with a computerized go/no-go task. The N2 amplitudes thought to tap inhibitory control were recorded, and a source analysis was conducted. In the second assessment, parents and children were videotaped while trying to solve a conflict topic. State space grids were used to derive two dynamic flexibility parameters from the coded videotapes: (a) the number of transitions between emotional states and (b) the dispersion of emotional states, based on proportional durations in each state. The regression results showed that flexibility measures were not related to N2 amplitudes. However, flexibility measures were significantly associated with the ratio of dorsal to ventral source activation: for transitions, ΔR2 = .27, F (1, 34) = 13.13, p = .001; for dispersion, ΔR2 = .29, F (1, 35) = 14.76, p < .001. Thus, in support of our main hypothesis, greater dyadic flexibility was associated with a higher ratio of dorsomedial to ventral activation, suggesting that children with more flexible parent–child interactions are able to recruit relatively more dorsomedial activity in challenging situations.

Type
Articles
Copyright
Copyright © Cambridge University Press 2012

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

Achenbach, T. M. (1991). Manual for the Child Behavior Checklist/4–18 and 1991 profile—Teacher version. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Bekker, E. M., Kenemans, J. L., & Verbaten, M. N. (2005). Source analysis of the N2 in a cued Go/NoGo task. Brain Research Cognitive Brain Research, 22, 221231.CrossRefGoogle Scholar
Bertrand, O., Perrin, F., & Pernier, J. (1985). A theoretical justification of the average reference in topographic evoked potential studies. Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section, 62, 462464.CrossRefGoogle ScholarPubMed
Blair, R. J. R. (2001). Advances in neuropsychiatry: Neurocognitive models of aggression, the antisocial personality disorders, and psychopathy. Journal of Neurology, Neurosurgery & Psychiatry, 71, 727731.CrossRefGoogle Scholar
Bögels, S. M., & Brechman-Toussaint, M. L. (2006). Family issues in child anxiety: Attachment, family functioning, parental rearing and beliefs. Clinical Psychology Review, 26, 834856.CrossRefGoogle ScholarPubMed
Bokura, H., Yamaguchi, S., & Kobayashi, S. (2001). Electrophysiological correlates for response inhibition in a Go/NoGo task. Clinical Neurophysiology, 112, 22242232.CrossRefGoogle Scholar
Bradley, S. (2003). Affect regulation and the development of psychopathology. New York: Guilford Press.Google Scholar
Bronfenbrenner, U., & Morris, P. A. (1998). The ecology of developmental processes. In Lerner, R. M. (Ed.), Handbook of child psychology: Vol. 1. Theoretical models of human development (Vol. 5, pp. 9931028). New York: Wiley.Google Scholar
Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences, 4, 215222.CrossRefGoogle ScholarPubMed
Bush, G., Vogt, B. A., Holmes, J., Dale, A. M., Greve, D., Jenike, M. A., et al. (2002). Dorsal anterior cingulate cortex: A role in reward-based decision making. Proceedings of the National Academy of Sciences, 99, 523528.CrossRefGoogle ScholarPubMed
Calkins, S. D. (1994). Origins and outcomes of individual differences in emotion regulation. Monographs of the Society for Research in Child Development, 59(2–3, Serial No. 240), 5372.CrossRefGoogle ScholarPubMed
Calkins, S. D., & Howse, R. B. (2004). Individual differences in self-regulation: Implications for childhood. In Philippot, P. & Feldman, R. S. (Eds.), The regulation of emotion. Mahwah, NJ: Erlbaum.Google Scholar
Carter, C. S., Macdonald, A. M., Botvinick, M., Ross, L. L., Stenger, V. A., Noll, D., et al. (2000). Parsing executive processes: Strategic vs. evaluative functions of the anterior cingulate cortex. Proceedings of the National Academy of Sciences, 97, 19441948.CrossRefGoogle ScholarPubMed
Cole, P. M., Martin, S. E., & Dennis, T. A. (2004). Emotion regulation as a scientific construct: Methodological challenges and directions for child development research. Child Development, 75, 317333.CrossRefGoogle ScholarPubMed
Cole, P. M., Michel, M. K., & Teti, L. O. (1994). The development of emotion regulation and dysregulation: A clinical perspective. Monographs of the Society for Research in Child Development, 59(2–3, Serial No. 240), 73100.CrossRefGoogle ScholarPubMed
Dadds, M. R., Barrett, P. M., Rapee, R. M., & Ryan, S. (1996). Family process and child anxiety and aggression: An observational analysis. Journal of Abnormal Child Psychology, 24, 715734.CrossRefGoogle ScholarPubMed
Dahl, R. (2003). Beyond raging hormones: The tinderbox in the teenage brain. Cerebrum: The Dana Forum on Brain Science, 5, 722.Google Scholar
Damasio, A. (1994). Decartes’ error: Emotion, reason, and the human brain. New York: Harper Collins.Google Scholar
Davidson, R. J., Jackson, D. C., & Kalin, N. H. (2000). Emotion, plasticity, context, and regulation: Perspectives from affective neuroscience. Psychological Bulletin, 126, 890909.CrossRefGoogle ScholarPubMed
Davidson, R. J., Putnam, K. M., & Larson, C. L. (2000). Dysfunction in the neural circuitry of emotion regulation—A possible prelude to violence. Science, 289, 591594.CrossRefGoogle ScholarPubMed
Diamond, A. (2002). Normal development of prefrontal cortex from birth to young adulthood: Cognitive functions, anatomy, and biochemistry. Principles of frontal lobe function. In Knight, S. A. (Ed.), The frontal lobes. London: Oxford University Press.Google Scholar
Drevets, W. C., & Raichle, M. E. (1998). Reciprocal suppression of regional cerebral blood flow during emotional versus higher cognitive processes: Implications for interactions between emotion and cognition. Cognition and Emotion, 12, 353385.CrossRefGoogle Scholar
Dumas, J. E., & LaFreniere, P. J. (1993). Mother–child relationships as sources of support or stress: A comparison of competent, average, aggressive, and anxious dyads. Child Development, 64, 17321754.CrossRefGoogle ScholarPubMed
Dumas, J. E., LaFreniere, P. J., & Serketich, W. J. (1995). “Balance of power”: A transactional analysis of control in mother–child dyads involving socially competent, aggressive, and anxious children. Journal of Abnormal Psychology, 104, 104113.CrossRefGoogle ScholarPubMed
Eisenberg, N., Cumberland, A., Spinrad, T. L., Fabes, R. A., Shepard, S. A., Reiser, M., et al. (2001). The relations of regulation and emotionality to children's externalizing and internalizing problem behavior. Child Development, 72, 11121134.CrossRefGoogle ScholarPubMed
Eisenberg, N., Spinrad, T. L., Fabes, R. A., Reiser, M., Cumberland, A., Shepard, S. A., et al. (2004). The relations of effortful control and impulsivity to children's resiliency and adjustment. Child Development, 75, 2546.CrossRefGoogle ScholarPubMed
Falkenstein, M., Hoormann, J., & Hohnsbein, J. (1999). ERP components in Go/Nogo tasks and their relation to inhibition. Acta Psychologica, 101, 267291.CrossRefGoogle ScholarPubMed
Fallgatter, A. J., & Strik, W. K. (1999). The NoGo-anteriorization as a neurophysiological standard-index for cognitive response control. International Journal of Psychophysiology, 32, 233238.CrossRefGoogle ScholarPubMed
Forgatch, M. S., & Degarmo, D. S. (1999). Two faces of Janus: Cohesion and conflict. In Brooks-Gunn, M. J. Cox (Ed.), Conflict and cohesion in families: Causes and consequences (pp. 167184). Mahwah, NJ: Erlbaum.Google Scholar
Garavan, H., Ross, T. J., & Stein, E. A. (1999). Right hemispheric dominance of inhibitory control: An event-related functional MRI study. Proceedings of the National Academy of Sciences, 96, 83018306.CrossRefGoogle ScholarPubMed
Gehring, W. J., Goss, B., Coles, M. G. H., Meyer, D. E., & Donchin, E. (1993). A neural system for error detection and compensation. Psychological Science, 4, 385390.CrossRefGoogle Scholar
Giedd, J. N., Blumenthal, J., Jeffries, N. O., Rajapakse, J. C., Vaituzis, A. C., Liu, H., et al. (1999). Development of the human corpus callosum during childhood and adolescence: A longitudinal MRI study. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 23, 571588.Google ScholarPubMed
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., et al. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences, 101, 81748179.CrossRefGoogle ScholarPubMed
Gottman, J. M., Katz, L. F., & Hooven, C. (1996). Parental meta-emotion philosophy and the emotional life of families: Theoretical models and preliminary data. Journal of Family Psychology, 10, 243268.CrossRefGoogle Scholar
Gottman, J. M., McCoy, K., Coan, J., & Collier, H. (1996). The Specific Affect Coding System (SPAFF) for observing emotional communication in marital and family interaction. Mahwah, NJ: Erlbaum.Google Scholar
Granic, I., & Lamey, A. V. (2002). Combining dynamic systems and multivariate analyses to compare the mother–child interactions of externalizing subtypes. Journal of Abnormal Child Psychology, 30, 265283.CrossRefGoogle ScholarPubMed
Granic, I., Hollenstein, T., Dishion, T. J., & Patterson, G. R. (2003). Longitudinal analysis of flexibility and reorganization in early adolescence: A dynamic systems study of family interactions. Developmental Psychology, 39, 606617.CrossRefGoogle ScholarPubMed
Granic, I., O'Hara, A., Pepler, D., & Lewis, M. D. (2007). A dynamic systems analysis of parent–child changes associated with successful “real-world” interventions for aggressive children. Journal of Abnormal Child Psychology, 35, 845857.CrossRefGoogle ScholarPubMed
Granic, I., & Patterson, G. R. (2006). Toward a comprehensive model of antisocial development: A dynamic systems approach. Psychological Review, 113, 101131.CrossRefGoogle Scholar
Gross, J. J. (1998a). Antecedent- and response-focused emotion regulation: Divergent consequences for experience, expression, and physiology. Journal of Personality and Social Psychology, 74, 224237.CrossRefGoogle ScholarPubMed
Gross, J. J. (1998b). The emerging field of emotion regulation: An integrative review. Review of General Psychology, 2, 271299.CrossRefGoogle Scholar
Hariri, A. R., Mattay, V. S., Tessitore, A., Fera, F., Weinberger, D. R., James, W., et al. (2003). Neocortical modulation of the amygdala response to fearful stimuli. Physiology & Behavior, 53, 494501Google ScholarPubMed
Hollenstein, T., Granic, I., Stoolmiller, M., & Snyder, J. (2004). Rigidity in parent–child interactions and the development of externalizing and internalizing behavior in early childhood. Journal of Abnormal Child Psychology, 32, 595607.CrossRefGoogle ScholarPubMed
Hoptman, M. J. (2003). Neuroimaging studies of violence and antisocial behavior. Journal of Psychiatric Practice, 9, 265278.CrossRefGoogle ScholarPubMed
Hum, K. M., & Lewis, M. D. (in press). Neural mechanisms of emotion regulation in children: Implications for normative development and emotion-related disorders. In Barrett, K. & Morgan, G. (Eds.), Handbook of self-regulatory processes in development: New directions and international perspectives. New York: Routledge.Google Scholar
Izard, C. E. (1977). Human emotions. New York: Plenum Press.CrossRefGoogle Scholar
Kashdan, T. B., & Rottenberg, J. (2010). Psychological flexibility as a fundamental aspect of health. Clinical Psychology Review, 30, 865878.CrossRefGoogle ScholarPubMed
Ladouceur, C. D., Dahl, R. E., Birmaher, B., Axelson, D. A., & Ryan, N. D. (2006). Increased error-related negativity (ERN) in childhood anxiety disorders: ERP and source localization. Journal of Child Psychology and Psychiatry, 47, 10731082.CrossRefGoogle ScholarPubMed
Lamm, C., Granic, I., Zelazo, P. D., & Lewis, M. D. (2011). Magnitude and chronometry of neural mechanisms of emotion regulation in subtypes of aggressive children. Brain and Cognition, 77, 159169.CrossRefGoogle ScholarPubMed
Levesque, J., Joanette, Y., Mensour, B., Beaudoin, G., Leroux, J. M., Bourgouin, P., et al. (2003). Neural correlates of sad feelings in healthy girls. Neuroscience, 121, 545551.CrossRefGoogle ScholarPubMed
Lewis, M. D. (2000). The promise of dynamic systems approaches for an integrated account of human development. Child Development, 71, 3643.CrossRefGoogle ScholarPubMed
Lewis, M. D., Granic, I., & Lamm, C. (2006). Behavioral differences in aggressive children linked with neural mechanisms of emotion regulation. Resilience in Children, 1094, 164177.Google ScholarPubMed
Lewis, M. D., Granic, I., Lamm, C., Zelazo, P. D., Stieben, J., Todd, R. M., et al. (2008). Changes in the neural bases of emotion regulation associated with clinical improvement in children with behavior problems. Development and Psychopathology, 20, 913939.CrossRefGoogle ScholarPubMed
Lewis, M. D., Lamey, A. V., & Douglas, L. (1999). A new dynamic systems method for the analysis of early socioemotional development. Developmental Science, 2, 458476.CrossRefGoogle Scholar
Lewis, M. D., Lamm, C., Segalowitz, S. J., Stieben, J., & Zelazo, P. D. (2006). Neurophysiological correlates of emotion regulation in children and adolescents. Journal of Cognitive Neuroscience, 18, 430443.CrossRefGoogle ScholarPubMed
Lunkenheimer, E. S., Olson, S. L., Hollenstein, T., Sameroff, A. J., & Winter, C. (2011). Dyadic flexibility and positive affect in parent–child coregulation and the development of child behavior problems. Development and Psychopathology, 23, 577591.CrossRefGoogle ScholarPubMed
Magai, C., & McFadden, S. H. (Eds.). (1995). The role of emotions in social and personality development: History, theory, and research. New York: Plenum Press.Google Scholar
Mayberg, H. S., Liotti, M., Brannan, S. K., McGinnis, S., Mahurin, R. K., Jerabek, P. A., et al. (1999). Reciprocal limbic–cortical function and negative mood: Converging PET findings in depression and normal sadness. American Journal of Psychiatry, 156, 675682.CrossRefGoogle ScholarPubMed
McClure, E. B., Monk, C. S., Nelson, E. E., Parrish, J. M., Adler, A., Blair, R. J., et al. (2007). Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Archives of General Psychiatry, 64, 97106.CrossRefGoogle ScholarPubMed
Michel, C. M., Murray, M. M., Lantz, G., Gonzalez, S., Spinelli, L., & Grave de Peralta, R. (2004). EEG source imaging. Clinical Neurophysiology, 115, 2195–222.CrossRefGoogle ScholarPubMed
Monk, C. S., Nelson, E. E., McClure, E. B., Mogg, K., Bradley, B. P., Leibenluft, E., et al. (2006). Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. American Journal of Psychiatry, 163, 10911097.CrossRefGoogle ScholarPubMed
Nieuwenhuis, S., Yeung, N., van den Wildenberg, W., & Ridderinkhof, K. R. (2003). Electrophysiological correlates of anterior cingulate function in a go/no-go task: Effects of response conflict and trial type frequency. Cognitive, Affective, & Behavioral Neuroscience, 3, 1726.CrossRefGoogle Scholar
Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D., et al. (2004). For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage, 23, 483499.CrossRefGoogle ScholarPubMed
Patterson, G. R. (1982). Coercive family process. Eugene, OR: Castilia.Google Scholar
Patterson, G. R., Reid, J., & Dishion, T. J. (1992). Antisocial boys. Eugene, OR: Castalia.Google Scholar
Paus, T. (2005). Mapping brain maturation and cognitive development during adolescence. Trends in Cognitive Sciences, 9, 6068.CrossRefGoogle ScholarPubMed
Pliszka, S. R., Liotti, M., & Woldorff, M. G. (2000). Inhibitory control in children with attention-deficit/hyperactivity disorder: Event-related potentials identify the processing component and timing of an impaired right-frontal response-inhibition mechanism. Biological Psychiatry, 48, 238246.CrossRefGoogle ScholarPubMed
Robin, A. L., & Weiss, J. G. (1980). Criterion-related validity of behavioral and self-report measures of problem-solving communication-skills in distressed and non-distressed parent–adolescent dyads. Behavioral Assessment, 2, 339352.Google Scholar
Rolls, E. (2004). The functions of the orbitofrontal cortex. Brain and Cognition, 55, 1129.CrossRefGoogle ScholarPubMed
Rothbart, M. K., Ahadi, S. A., & Hershey, K. L. (1994). Temperament and social behavior in childhood. Journal of Developmental Psychology, 40, 2139.Google Scholar
Rothbart, M. K., & Bates, J. E. (1998). Temperament. In Damon, W. & Lerner, R. M. (Eds.), Handbook of child psychology (pp. 105176). New York: Wiley.Google Scholar
Snyder, J., & Patterson, G. (1995). Individual differences in social aggression: A test of a reinforcement model of socialization in the natural environment. Behavior Therapy, 26, 371391.CrossRefGoogle Scholar
Southam-Gerow, M. A., & Kendall, P. C. (2002). Emotion regulation and understanding—Implications for child psychopathology and therapy. Clinical Psychology Review, 22, 189222.CrossRefGoogle Scholar
Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417463.CrossRefGoogle ScholarPubMed
Stadler, C., Sterzer, P., Schmeck, K., Krebs, A., Kleinschmidt, A., & Poustka, F. (2007). Reduced anterior cingulate activation in aggressive children and adolescents during affective stimulation: Association with temperament traits. Journal of Psychiatric Research, 41, 410417.CrossRefGoogle ScholarPubMed
Steinberg, L. D. (2005). Cognitive and affective development in adolescence. Trends in Cognitive Sciences, 9, 6974.CrossRefGoogle ScholarPubMed
Sterzer, P., Stadler, C., Krebs, A., Kleinschmidt, A., & Poustka, F. (2005). Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder. Biological Psychiatry, 57, 715.CrossRefGoogle ScholarPubMed
Stieben, J., Lewis, M. D., Granic, I., Zelazo, P. D., Segalowitz, S., & Pepler, D. (2007). Neurophysiological mechanisms of emotion regulation for subtypes of externalizing children. Development and Psychopathology, 19, 455480.CrossRefGoogle ScholarPubMed
Tomkins, S. S. (1963). Affect, imagery, consciousness: Vol. 11. The negative affects. New York: Springer.Google Scholar
Tucker, D. M., Liotti, M., Potts, G. F., Russell, G. S., & Posner, M. I. (1994). Spatiotemporal analysis of brain electrical fields. Human Brain Mapping, 1, 134152.CrossRefGoogle Scholar
van Gaal, S., Lamme, V. A. F., Fahrenfort, J. J., & Ridderinkhof, K. R. (2011). Dissociable brain mechanisms underlying the conscious and unconscious control of behavior. Journal of Cognitive Neuroscience, 23, 91105.CrossRefGoogle ScholarPubMed
van Goozen, S. H. M., Fairchild, G., Snoek, H., & Harold, G. T. (2007). The evidence for a neurobiological model of childhood behavior. Psychological Bulletin, 133, 149182.CrossRefGoogle Scholar
van Veen, V., & Carter, C. S. (2002). The anterior cingulate as a conflict monitor: fMRI and ERP studies. Physiology & Behavior, 77, 477482.CrossRefGoogle ScholarPubMed
van Veen, V., Cohen, J. D., Botvinick, M. M., Stenger, V. A., & Carter, C. S. (2001). Anterior cingulate cortex, conflict monitoring, and levels of processing. NeuroImage, 14, 13021308.CrossRefGoogle ScholarPubMed
Woltering, S., Granic, I., Lamm, C., & Lewis, M. D. (2011). Neural changes associated with treatment outcome in children with externalizing problems. Biological Psychiatry, 70, 879–873.CrossRefGoogle ScholarPubMed
Zelazo, P. D., & Cunningham, W. A. (2007). Executive function—Mechanisms underlying emotion regulation. In Gross, J. (Ed.), Handbook of emotion regulation (pp. 135158). New York: Guilford Press.Google Scholar
Zhou, Q., Hofer, C., Eisenberg, N., Reiser, M., Spinrad, T. L., & Fabes, R. A. (2007). The developmental trajectories of attention focusing, attentional and behavioral persistence, and externalizing problems during school-age years. Developmental Psychology, 43, 369385.CrossRefGoogle ScholarPubMed