Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-23T13:33:37.443Z Has data issue: false hasContentIssue false
  • English
  • Français

Altered intrinsic functional connectivity of the cingulate cortex in children with severe temper outbursts

Published online by Cambridge University Press:  14 August 2017

Amy Krain Roy ,
Randi Bennett ,
Jonathan Posner ,
Leslie Hulvershorn ,
F. Xavier Castellanos  and
Rachel G. Klein
Amy Krain Roy*
Affiliation:
Fordham University New York University Langone School of Medicine
Randi Bennett
Affiliation:
Fordham University
Jonathan Posner
Affiliation:
Columbia University College of Physicians and Surgeons New York State Psychiatric Institute
Leslie Hulvershorn
Affiliation:
Indiana University School of Medicine
F. Xavier Castellanos
Affiliation:
New York University Langone School of Medicine
Rachel G. Klein
Affiliation:
New York University Langone School of Medicine
*
Address correspondence and reprint requests to: Amy Krain Roy, Dealy Hall 418, Fordham University, 441 East Fordham Road, Bronx, NY 10458; E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

Severe temper outbursts (STO) in children are associated with impaired school and family functioning and may contribute to negative outcomes. These outbursts can be conceptualized as excessive frustration responses reflecting reduced emotion regulation capacity. The anterior cingulate cortex (ACC) has been implicated in negative affect as well as emotional control, and exhibits disrupted function in children with elevated irritability and outbursts. This study examined the intrinsic functional connectivity (iFC) of a region of the ACC, the anterior midcingulate cortex (aMCC), in 5- to 9-year-old children with STO (n = 20), comparing them to children with attention-deficit/hyperactivity disorder (ADHD) without outbursts (ADHD; n = 18). Additional analyses compared results to a sample of healthy children (HC; n = 18) and examined specific associations with behavioral and emotional dysregulation. Compared to the ADHD group, STO children exhibited reduced iFC between the aMCC and surrounding regions of the ACC, and increased iFC between the aMCC and precuneus. These differences were also seen between the STO and HC groups; ADHD and HC groups did not differ. Specificity analyses found associations between aMCC–ACC connectivity and hyperactivity, and between aMCC–precuneus iFC and emotion dysregulation. Disruption in aMCC networks may underlie the behavioral and emotional dysregulation characteristic of children with STO.

Type
Regular Articles
Information
Development and Psychopathology , Volume 30 , Issue 2 , May 2018 , pp. 571 - 579
Copyright
Copyright © Cambridge University Press 2017 

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.)

Footnotes

We thank Aleta Angelosante, Vasco Lopes, and Sheina Godovich, as well as our participants and their families for their contributions to this research. This work was supported by a Brain and Behavior Research Foundation (previously NARSAD) Young Investigator Award (to A.K.R.), Grant R01MH091140 from the National Institute of Mental Health (A.K.R., Principal Investigator), a grant from the Seevak Family Foundation (R.G.K., Principal Investigator), and an AACAP Pilot Research Award for Junior Faculty and Child and Adolescent Psychiatry Residents, supported by the Elaine Schlosser Lewis Fund (to L.H.).

References

Abler, B., Walter, H., & Erk, S. (2005). Neural correlates of frustration. NeuroReport, 16, 669–672.Google Scholar
Avants, B. B., Tustison, N. J., Song, G., Cook, P. A., Klein, A., & Gee, J. C. (2011). A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage, 54, 2033–2044. doi:10.1016/j.neuroimage.2010.09.025Google Scholar
Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage, 37, 90–101.Google Scholar
Bhatia, M. S., Nigam, V. R., Bohra, N., & Malik, S. C. (1991). Attention deficit disorder with hyperactivity among paediatric outpatients. Journal of Child Psychology and Psychiatry, 32, 297–306.Google Scholar
Bonath, B., Tegelbeckers, J., Wilke, M., Flechtner, H. H., & Krauel, K. (2016). Regional gray matter volume differences between adolescents with ADHD and typically developing controls: Further evidence for anterior cingulate involvement. Journal of Attention Disorders. Advance online publication. doi:10.1177/1087054715619682Google Scholar
Brotman, M. A., Schmajuk, M., Rich, B. A., Dickstein, D. P., Guyer, A. E., Costello, E. J., … Leibenluft, E. (2006). Prevalence, clinical correlates, and longitudinal course of severe mood dysregulation in children. Biological Psychiatry, 60, 991–997. doi:10.1016/j.biopsych.2006.08.042Google Scholar
Burke, J. D., Hipwell, A. E., & Loeber, R. (2010). Dimensions of oppositional defiant disorder as predictors of depression and conduct disorder in preadolescent girls. Journal of the American Academy of Child & Adolescent Psychiatry, 49, 484–492.Google Scholar
Bush, G., Valera, E. M., & Seidman, L. J. (2005). Functional neuroimaging of attention-deficit/hyperactivity disorder: A review and suggested future directions. Biological Psychiatry, 57, 1273–1284. doi:10.1016/j.biopsych.2005.01.034Google Scholar
Carlson, G. A., Potegal, M., Margulies, D., Gutkovich, Z., & Basile, J. (2009). Rages—What are they and who has them? Journal of Child and Adolescent Psychopharmacology, 19, 281–288.Google Scholar
Castellanos, F. X., Margulies, D. S., Kelly, C., Uddin, L. Q., Ghaffari, M., Kirsch, A., … Milham, M. P. (2008). Cingulate-precuneus interactions: A new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biological Psychiatry, 63, 332–337.Google Scholar
Cortese, S., Kelly, C., Chabernaud, C., Proal, E., Di Martino, A., Milham, M. P., & Castellanos, F. X. (2012). Toward systems neuroscience of ADHD: A meta-analysis of 55 fMRI studies. American Journal of Psychiatry, 169, 1038–1055. doi:10.1176/appi.ajp.2012.11101521Google Scholar
Deveney, C. M., Connolly, M. E., Haring, C. T., Bones, B. L., Reynolds, R. C., Kim, P., … Leibenluft, E. (2013). Neural mechanisms of frustration in chronically irritable children. American Journal of Psychiatry, 170, 1186–1194. doi:10.1176/appi.ajp.2013.12070917Google Scholar
Dickstein, S. G., Bannon, K., Castellanos, F. X., & Milham, M. P. (2006). The neural correlates of attention deficit hyperactivity disorder: An ALE meta-analysis. Journal of Child Psychology and Psychiatry, 47, 1051–1062. doi:10.1111/j.1469-7610.2006.01671.xGoogle Scholar
Dominick, K. C., Davis, N. O., Lainhart, J., Tager-Flusberg, H., & Folstein, S. (2007). Atypical behaviors in children with autism and children with a history of language impairment. Research in Developmental Disabilities, 28, 145–162. doi:10.1016/j.ridd.2006.02.003Google Scholar
Fair, D. A., Dosenbach, N. U., Church, J. A., Cohen, A. L., Brahmbhatt, S., Miezin, F. M., … Schlaggar, B. L. (2007). Development of distinct control networks through segregation and integration. Proceedings of the National Academy of Sciences, 104, 13507–13512. doi:10.1073/pnas.0705843104Google Scholar
Francx, W., Oldehinkel, M., Oosterlaan, J., Heslenfeld, D., Hartman, C. A., Hoekstra, P. J., … Mennes, M. (2015). The executive control network and symptomatic improvement in attention-deficit/hyperactivity disorder. Cortex, 73, 62–72. doi:10.1016/j.cortex.2015.08.012Google Scholar
Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., & Turner, R. (1996). Movement-related effects in fMRI time-series. Magnetic Resonance Medicine, 35, 346–355.Google Scholar
Gatzke-Kopp, L. M., Greenberg, M., & Bierman, K. (2015). Children's parasympathetic reactivity to specific emotions moderates response to intervention for early-onset aggression. Journal of Clinical Child and Adolescent Psychology, 44, 291–304. doi:10.1080/15374416.2013.862801Google Scholar
Giesbrecht, G. F., Miller, M. R., & Muller, U. (2010). The anger-distress model of temper tantrums: Associations with emotional reactivity and emotional competence. Infant and Child Development, 19, 478–497.Google Scholar
Greve, D. N., & Fischl, B. (2009). Accurate and robust brain image alignment using boundary-based registration. NeuroImage, 48, 63–72. doi:10.1016/j.neuroimage.2009.06.060Google Scholar
He, J., Jin, X., Zhang, M., Huang, X., Shui, R., & Shen, M. (2013). Anger and selective attention to reward and punishment in children. Journal of Experimental Child Psychology, 115, 389–404. doi:10.1016/j.jecp.2013.03.004Google Scholar
Johnco, C., Salloum, A., De Nadai, A. S., McBride, N., Crawford, E. A., Lewin, A. B., & Storch, E. A. (2015). Incidence, clinical correlates and treatment effect of rage in anxious children. Psychiatry Research, 229, 63–69. doi:10.1016/j.psychres.2015.07.071Google Scholar
Kanske, P., Heissler, J., Schonfelder, S., Bongers, A., & Wessa, M. (2011). How to regulate emotion? Neural networks for reappraisal and distraction. Cerebral Cortex, 21, 1379–1388. doi:10.1093/cercor/bhq216Google Scholar
Kaufman, A. S., & Kaufman, N. L. (2004). Kaufman Brief Intelligence Test—Second edition (KBIT-2). Circle Pines, MN: American Guidance Service.Google Scholar
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., … Ryan, N. (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children—Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 980–988.Google Scholar
Kelly, A. M., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., … Milham, M. P. (2008). Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cerebral Cortex, 19, 640–657. doi:10.1093/cercor/bhn117Google Scholar
Leibenluft, E., Cohen, P., Gorrindo, T., Brook, J. S., & Pine, D. S. (2006). Chronic versus episodic irritability in youth: A community-based, longitudinal study of clinical and diagnostic associations. Journal of Child and Adolescent Psychopharmacology, 16, 456–466. doi:10.1089/cap.2006.16.456Google Scholar
Makris, N., Buka, S. L., Biederman, J., Papadimitriou, G. M., Hodge, S. M., Valera, E. M., … Seidman, L. J. (2008). Attention and executive systems abnormalities in adults with childhood ADHD: A DT-MRI study of connections. Cerebral Cortex, 18, 1210–1220. doi:10.1093/cercor/bhm156Google Scholar
Malone, R. P., Gratz, S. S., Delaney, M. A., & Hyman, S. B. (2005). Advances in drug treatments for children and adolescents with autism and other pervasive developmental disorders. CNS Drugs, 19, 923–934.Google Scholar
Margulies, D. S., Kelly, A. M., Uddin, L. Q., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2007). Mapping the functional connectivity of anterior cingulate cortex. NeuroImage, 37, 579–588. doi:10.1016/j.neuroimage.2007.05.019Google Scholar
McRae, K., Hughes, B., Chopra, S., Gabrieli, J. D., Gross, J. J., & Ochsner, K. N. (2010). The neural bases of distraction and reappraisal. Journal of Cognitive Neuroscience, 22, 248–262. doi:10.1162/jocn.2009.21243Google Scholar
Pawliczek, C. M., Derntl, B., Kellermann, T., Gur, R. C., Schneider, F., & Habel, U. (2013). Anger under control: Neural correlates of frustration as a function of trait aggression. PLOS ONE, 8, e78503. doi:10.1371/journal.pone.0078503Google Scholar
Perlman, S. B., Jones, B. M., Wakschlag, L. S., Axelson, D., Birmaher, B., & Phillips, M. L. (2015). Neural substrates of child irritability in typically developing and psychiatric populations. Developmental Cognitive Neuroscience, 14, 71–80. doi:10.1016/j.dcn.2015.07.003Google Scholar
Potegal, M., & Davidson, R. J. (2003). Temper tantrums in young children: 1. Behavioral composition. Journal of Developmental and Behavioral Pediatrics, 24, 140–147.Google Scholar
Reynolds, C. R., & Kamphaus, R. W. (2004). Behavior Assessment System for Children (2nd ed.). Circle Pines, MN: American Guidance Service.Google Scholar
Rich, B. A., Carver, F. W., Holroyd, T., Rosen, H. R., Mendoza, J. K., Cornwell, B. R., … Leibenluft, E. (2011). Different neural pathways to negative affect in youth with pediatric bipolar disorder and severe mood dysregulation. Journal of Psychiatric Research, 45, 1283–1294. doi:10.1016/j.jpsychires.2011.04.006Google Scholar
Rich, B. A., Schmajuk, M., Perez-Edgar, K. E., Fox, N. A., Pine, D. S., & Leibenluft, E. (2007). Different psychophysiological and behavioral responses elicited by frustration in pediatric bipolar disorder and severe mood dysregulation. American Journal of Psychiatry, 164, 309–317. doi:10.1176/ajp.2007.164.2.309Google Scholar
Rilling, J. K., Goldsmith, D. R., Glenn, A. L., Jairam, M. R., Elfenbein, H. A., Dagenais, J. E., … Pagnoni, G. (2008). The neural correlates of the affective response to unreciprocated cooperation. Neuropsychologia, 46, 1256–1266. doi:10.1016/j.neuropsychologia.2007.11.033Google Scholar
Rowe, R., Costello, E. J., Angold, A., Copeland, W. E., & Maughan, B. (2010). Developmental pathways in oppositional defiant disorder and conduct disorder. Journal of Abnormal Psychology, 119, 726–738. doi:10.1037/a0020798Google Scholar
Roy, A. K., Klein, R. G., Angelosante, A., Bar-Haim, Y., Leibenluft, E., Hulvershorn, L., … Spindel, C. (2013). Clinical features of young children referred for impairing temper outbursts. Journal of Child and Adolescent Psychopharmacology, 23, 588–596. doi:10.1089/cap.2013.0005Google Scholar
Sato, J. R., Salum, G. A., Gadelha, A., Picon, F. A., Pan, P. M., Vieira, G., … Jackowski, A. P. (2014). Age effects on the default mode and control networks in typically developing children. Journal of Psychiatric Research, 58, 89–95. doi:10.1016/j.jpsychires.2014.07.004Google Scholar
Seidman, L. J., Valera, E. M., Makris, N., Monuteaux, M. C., Boriel, D. L., Kelkar, K., … Biederman, J. (2006). Dorsolateral prefrontal and anterior cingulate cortex volumetric abnormalities in adults with attention-deficit/hyperactivity disorder identified by magnetic resonance imaging. Biological Psychiatry, 60, 1071–1080. doi:10.1016/j.biopsych.2006.04.031Google Scholar
Shackman, A. J., Salomons, T. V., Slagter, H. A., Fox, A. S., Winter, J. J., & Davidson, R. J. (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews Neuroscience, 12, 154–167. doi:10.1038/nrn2994Google Scholar
Shields, A., & Cicchetti, D. (1997). Emotion regulation among school-age children: The development and validation of a new criterion Q-sort scale. Developmental Psychology, 33, 906–916.Google Scholar
Siegrist, J., Menrath, I., Stocker, T., Klein, M., Kellermann, T., Shah, N. J., … Schneider, F. (2005). Differential brain activation according to chronic social reward frustration. NeuroReport, 16, 1899–1903.Google Scholar
Spunt, R. P., Lieberman, M. D., Cohen, J. R., & Eisenberger, N. I. (2012). The phenomenology of error processing: The dorsal ACC response to stop-signal errors tracks reports of negative affect. Journal of Cognitive Neuroscience, 24, 1753–1765. doi:10.1162/jocn_a_00242Google Scholar
Stoddard, J., Gotts, S. J., Brotman, M. A., Lever, S., Hsu, D., Zarate, C., … Leibenluft, E. (2016). Aberrant intrinsic functional connectivity within and between corticostriatal and temporal-parietal networks in adults and youth with bipolar disorder. Psychological Medicine, 46, 1509–1522. doi:10.1017/S0033291716000143Google Scholar
Stringaris, A., Cohen, P., Pine, D. S., & Leibenluft, E. (2009). Adult outcomes of youth irritability: A 20-year prospective community-based study. American Journal of Psychiatry, 166, 1048–1054. doi:10.1176/appi.ajp.2009.08121849Google Scholar
Stringaris, A., & Goodman, R. (2009). Longitudinal outcome of youth oppositionality: Irritable, headstrong, and hurtful behaviors have distinctive predictions. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 404–412. doi:10.1097/CHI.0b013e3181984f30Google Scholar
Sun, L., Cao, Q., Long, X., Sui, M., Cao, X., Zhu, C., … Wang, Y. (2012). Abnormal functional connectivity between the anterior cingulate and the default mode network in drug-naive boys with attention deficit hyperactivity disorder. Psychiatry Research, 201, 120–127. doi:10.1016/j.psychres.2011.07.001Google Scholar
Swingler, M. M., Perry, N. B., & Calkins, S. D. (2015). Neural plasticity and the development of attention: Intrinsic and extrinsic influences. Development and Psychopathology, 27, 443–457. doi:10.1017/S0954579415000085Google Scholar
Wakschlag, L. S., Choi, S. W., Carter, A. S., Hullsiek, H., Burns, J., McCarthy, K., … Briggs-Gowan, M. J. (2012). Defining the developmental parameters of temper loss in early childhood: Implications for developmental psychopathology. Journal of Child Psychology and Psychiatry, 53, 1099–1108. doi:10.1111/j.1469-7610.2012.02595.xGoogle Scholar
Xie, X., Mulej Bratec, S., Schmid, G., Meng, C., Doll, A., Wohlschlager, A., … Sorg, C. (2016). How do you make me feel better? Social cognitive emotion regulation and the default mode network. NeuroImage, 134, 270–280. doi:10.1016/j.neuroimage.2016.04.015Google Scholar
Yu, R., Mobbs, D., Seymour, B., Rowe, J. B., & Calder, A. J. (2014). The neural signature of escalating frustration in humans. Cortex, 54, 165–178. doi:10.1016/j.cortex.2014.02.013Google Scholar