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Inhibitory control and emotion dysregulation: A framework for research on anxiety

Published online by Cambridge University Press:  10 April 2019

Elise M. Cardinale*
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Anni R. Subar
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Melissa A. Brotman
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Ellen Leibenluft
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Katharina Kircanski
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Daniel S. Pine
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
*
Author for correspondence: Elise M. Cardinale, National Institute of Mental Health, Bldg. 15K, MSC 2670, Bethesda, MD 20892-2670; E-mail: elise.cardinale@nih.gov.

Abstract

While emotional dysregulation is a broad construct, the current paper adopts a narrow approach to facilitate translational neuroscience research on pediatric anxiety. The paper first presents data on an adapted version of the antisaccade task and then integrates these data into a research framework. Data on an adapted version of the antisaccade task were collected in 57 youth, including 35 seeking treatment for an anxiety disorder. Associations were examined between performance on the antisaccade task and (a) age, (b) performance on other cognitive-control tasks (i.e., the stop-signal delay and flanker tasks), and (c) level of anxiety symptoms. Better performance on the antisaccade task occurred in older relative to younger subjects and correlated with better performance on the flanker task. Across the 57 youth, higher levels of anxiety correlated with shorter latency for correct antisaccades. These data can be placed within a three-step framework for translational neuroscience research. In the first step, a narrow index of emotion dysregulation is targeted. In the second step, this narrow index is linked to other correlated indicators of the same underlying narrow latent construct. In the third and final step, associations are examined with clinical outcomes and response to treatment.

Type
Special Issue Articles
Copyright
Copyright © Cambridge University Press 2019 

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References

Abend, R., de Voogd, L., Salemink, E., Wiers, R. W., Perez-Edgar, K., Fitzgerald, A., … Bar-Haim, Y. (2018). Association between attention bias to threat and anxiety symptoms in children and adolescents. Depression and Anxiety, 35, 229238. doi:10.1002/da.22706Google Scholar
Aichert, D. S., Wostmann, N. M., Costa, A., Macare, C., Wenig, J. R., Moller, H. J., … Ettinger, U. (2012). Associations between trait impulsivity and prepotent response inhibition. Journal of Clinical and Experimental Neuropsychology, 34, 10161032. doi:10.1080/13803395.2012.706261Google Scholar
Aldao, A., Gee, D. G., De Los Reyes, A., & Seager, I. (2016). Emotion regulation as a transdiagnostic factor in the development of internalizing and externalizing psychopathology: Current and future directions. Development and Psychopathology, 28(4, Pt. 1), 927946. doi:10.1017/S0954579416000638Google Scholar
Aron, A. R. (2011). From reactive to proactive and selective control: Developing a richer model for stopping inappropriate responses. Biological Psychiatry, 69, e55e68. doi:10.1016/j.biopsych.2010.07.024Google Scholar
Bari, A., & Robbins, T. W. (2013). Inhibition and impulsivity: Behavioral and neural basis of response control. Progress in Neurobiology, 108, 4479. doi:10.1016/j.pneurobio.2013.06.005Google Scholar
Beauchaine, T. P. (2015). Future directions in emotion dysregulation and youth psychopathology. Journal of Clinical Child and Adolescent Psychology, 44, 875896. doi:10.1080/15374416.2015.1038827Google Scholar
Beauchaine, T. P., & Zisner, A. (2017). Motivation, emotion regulation, and the latent structure of psychopathology: An integrative and convergent historical perspective. International Journal of Psychophysiology, 119, 108118. doi:10.1016/j.ijpsycho.2016.12.014Google Scholar
Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., & Neer, S. M. (1997). The Screen for Child Anxiety Related Emotional Disorders (SCARED): Scale construction and psychometric characteristics. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 545553. doi:10.1097/00004583-199707000-00021Google Scholar
Brotman, M. A., Kircanski, K., & Leibenluft, E. (2017). Irritability in children and adolescents. Annual Review of Clinical Psychology, 13, 317341. doi:10.1146/annurev-clinpsy-032816-044941Google Scholar
Cardinale, E. M., Breeden, A. L., Robertson, E. L., Lozier, L. M., Vanmeter, J. W., & Marsh, A. A. (2018). Externalizing behavior severity in youths with callous–unemotional traits corresponds to patterns of amygdala activity and connectivity during judgments of causing fear. Development and Psychopathology, 30, 191201. doi:10.1017/S0954579417000566Google Scholar
Cole, P. M., Hall, S. E., & Hajal, N. J. (2017). Emotion dysregulation as a vulnerability to psychopathology. In Beauchaine, T. P. & Hinshaw, S. P. (Eds.), Child and adolescent psychopathology (3rd ed., pp. 346386). Hoboken, NJ: Wiley.Google Scholar
Derakshan, N., Ansari, T. L., Hansard, M., Shoker, L., & Eysenck, M. W. (2009). Anxiety, inhibition, efficiency, and effectiveness: An investigation using antisaccade task. Experimental Psychology, 56, 4855. doi:10.1027/1618-3169.56.1.48Google Scholar
Eriksen, C. W. (1995). The flankers task and response competition: A useful tool for investigating a variety of cognitive problems. Visual Cognition, 2, 101118. doi:10.1080/13506289508401726Google Scholar
Everling, S., & Fischer, B. (1998). The antisaccade: A review of basic research and clinical studies. Neuropsychologia, 36, 885899. doi:10.1016/S0028-3932(98)00020-7Google Scholar
Fischer, B., & Ramsperger, E. (1984). Human express saccades: Extremely short reaction times of goal-directed eye movements. Experimental Brain Research, 57, 191195. doi:10.1007/BF00231145Google Scholar
Fox, N. A., & Calkins, S. D. (2003). The development of self-control of emotion: Intrinsic and extrinsic influences. Motivation and Emotion, 27, 726. doi:10.1023/A:1023622324898Google Scholar
Geier, C. F., & Luna, B. (2012). Developmental effects of incentives on response inhibition. Child Development, 83, 12621274. doi:10.1111/j.1467-8624.2012.01771.xGoogle Scholar
Gilliom, M., & Shaw, D. S. (2004). Codevelopment of externalizing and internalizing problems in early childhood. Development and Psychopathology, 16, 313333. https://doi.org/10.1017/S0954579404044530Google Scholar
Gold, A. L., Shechner, T., Farber, M. J., Spiro, C. N., Leibenluft, E., Pine, D. S., & Britton, J. C. (2016). Amygdala-cortical connectivity: Associations with anxiety, development, and threat: 2015 ADAA Scientific Research Symposium: Anxiety, development, and connectivity. Depression and Anxiety, 33, 917926. doi:10.1002/da.22470Google Scholar
Hallett, P. E. (1978). Primary and secondary saccades to goals defined by instructions. Vision Research, 18, 12791296. doi:10.1016/0042-6989(78)90218-3Google Scholar
Hardin, M. G., Mandell, D., Mueller, S. C., Dahl, R. E., Pine, D. S., & Ernst, M. (2009). Inhibitory control in anxious and healthy adolescents is modulated by incentive and incidental affective stimuli. Journal of Child Psychology and Psychiatry, 50, 15501558. doi: 10.1111/j.1469-7610.2009.02121.xGoogle Scholar
Hedge, C., Powell, G., & Sumner, P. (2018). The reliability paradox: Why robust cognitive tasks do not produce reliable individual differences. Behavior Research Methods, 50, 11661186. doi:10.3758/s13428-017-0935-1Google Scholar
Henderson, H. A., Pine, D. S., & Fox, N. A. (2015). Behavioral inhibition and developmental risk: A dual-processing perspective. Neuropsychopharmacology, 40, 207224. doi:10.1038/npp.2014.189Google Scholar
Hikosaka, O. (2007). Basal ganglia mechanisms of reward-oriented eye movement. Annals of the New York Academy of Sciences, 1104, 229249. doi:10.1196/annals.1390.012Google Scholar
Hikosaka, O., Kim, H. F., Amita, H., Yasuda, M., Isoda, M., Tachibana, Y., & Yoshida, A. (2018). Direct and indirect pathways for choosing objects and actions. European Journal of Neuroscience. Advance online publication. doi:10.1111/ejn.13876Google Scholar
Hiser, J., & Koenigs, M. (2018). The multifaceted role of the ventromedial prefrontal cortex in emotion, decision making, social cognition, and psychopathology. Biological Psychiatry, 83, 638647. doi:10.1016/j.biopsych.2017.10.030Google Scholar
Hofmann, S. G., Sawyer, A. T., Fang, A., & Asnaani, A. (2012). Review: Emotion Dysregulation Model of Mood and Anxiety Disorders. Depression and Anxiety, 29, 409416. doi:10.1002/da.21888Google Scholar
Hutton, S. B., & Ettinger, U. (2006). The antisaccade task as a research tool in psychopathology: A critical review. Psychophysiology, 43, 302313. doi:10.1111/j.1469-8986.2006.00403.xGoogle Scholar
Jazaieri, H., Morrison, A. S., Goldin, P. R., & Gross, J. J. (2015). The role of emotion and emotion regulation in social anxiety disorder. Current Psychiatry Reports, 17. doi:10.1007/s11920-014-0531-3Google Scholar
Kaufman, J., Birmaher, B., Brent, D., Rao, U. M. A., 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, 980988. doi:10.1097/00004583-199707000-00021Google Scholar
Kircanski, K., White, L. K., Tseng, W.-L., Wiggins, J. L., Frank, H. R., Sequeira, S., … Brotman, M. A. (2018). A latent variable approach to differentiating neural mechanisms of irritability and anxiety in youth. JAMA Psychiatry, 75, 631. doi:10.1001/jamapsychiatry.2018.0468Google Scholar
Kohn, N., Eickhoff, S. B., Scheller, M., Laird, A. R., Fox, P. T., & Habel, U. (2014). Neural network of cognitive emotion regulation—An ALE meta-analysis and MACM analysis. NeuroImage, 87, 345355. doi:10.1016/j.neuroimage.2013.11.001Google Scholar
LeDoux, J., & Daw, N. D. (2018). Surviving threats: Neural circuit and computational implications of a new taxonomy of defensive behaviour. Nature Reviews Neuroscience, 19, 269282. doi:10.1038/nrn.2018.22Google Scholar
LeDoux, J. E., & Pine, D. S. (2016). Using neuroscience to help understand fear and anxiety: A two-system framework. American Journal of Psychiatry, 173, 10831093. doi:10.1176/appi.ajp.2016.16030353Google Scholar
Loe, I. M., Feldman, H. M., Yasui, E., & Luna, B. (2009). Oculomotor performance identifies underlying cognitive deficits in attention-deficit/hyperactivity disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 431440. doi:10.1097/CHI.0b013e31819996daGoogle Scholar
Logan, G. D., & Cowan, W. B. (1984). On the ability to inhibit simple and choice reaction time responses: A model and a method. Journal of Experimental Psychology: Human Perception and Performance, 10, 276291.Google Scholar
Luna, B., Garver, K. E., Urban, T. A., Lazar, N. A., & Sweeney, J. A. (2004). Maturation of cognitive processes from late childhood to adulthood. Child Development, 75, 13571372. doi:10.1111/j.1467-8624.2004.00745.xGoogle Scholar
Luna, B., Velanova, K., & Geier, C. F. (2008). Development of eye-movement control. Brain and Cognition, 68, 293308. doi:10.1016/j.bandc.2008.08.019Google Scholar
Meyer, A., Hajcak, G., Torpey-Newman, D., Kujawa, A., Olino, T. M., Dyson, M., & Klein, D. N. (2018). Early temperamental fearfulness and the developmental trajectory of error-related brain activity. Developmental Psychobiology, 60, 224231. doi:10.1002/dev.21605Google Scholar
Miyake, A., & Friedman, N. P. (2012). The nature and organization of individual differences in executive functions: Four general conclusions. Current Directions in Psychological Science, 21, 814. doi:10.1177/0963721411429458Google Scholar
Moser, J. S., Moran, T. P., Schroder, H. S., Donnellan, M. B., & Yeung, N. (2013). On the relationship between anxiety and error monitoring: A meta-analysis and conceptual framework. Frontiers in Human Neuroscience, 7. doi:10.3389/fnhum.2013.00466Google Scholar
Mueller, S. C., Hardin, M. G., Korelitz, K., Daniele, T., Bemis, J., Dozier, M., … Ernst, M. (2012). Incentive effect on inhibitory control in adolescents with early-life stress: An antisaccade study. Child Abuse & Neglect, 36, 217225. doi:10.1016/j.chiabu.2011.10.010Google Scholar
Mueller, S. C., Hardin, M. G., Mogg, K., Benson, V., Bradley, B. P., Reinholdt-Dunne, M. L., … Ernst, M. (2012). The influence of emotional stimuli on attention orienting and inhibitory control in pediatric anxiety. Journal of Child Psychology and Psychiatry, 53, 856863. doi:10.1111/j.1469-7610.2012.02541.xGoogle Scholar
Musser, E. D., Galloway-Long, H. S., Frick, P. J., & Nigg, J. T. (2013). Emotion regulation and heterogeneity in attention-deficit/hyperactivity disorder. Journal of the Amerian Academy of Child & Adolescent Psychiatry, 52, 163171. doi:10.1016/j.jaac.2012.11.009Google Scholar
Nieuwenhuis, S., Broerse, A., Nielen, M. M., & de Jong, R. (2004). A goal activation approach to the study of executive function: An application to antisaccade tasks. Brain and Cognition, 56, 198214. doi:10.1016/j.bandc.2003.12.002Google Scholar
Nigg, J. T. (2013). Attention deficits and hyperactivity–impulsivity: What have we learned, what next? Development and Psychopathology, 25(4, Pt. 2), 14891503. doi:10.1017/S0954579413000734Google Scholar
Nigg, J. T. (2017). Annual Research Review: On the relations among self-regulation, self-control, executive functioning, effortful control, cognitive control, impulsivity, risk-taking, and inhibition for developmental psychopathology. Journal of Child Psychology and Psychiatry, 58, 3683. doi:10.1111/jcpp.12675Google Scholar
Ochsner, K. N., Silvers, J. A., & Buhle, J. T. (2012). A synthetic review and evolving model of the cognitive control of emotion: Functional imaging studies of emotion regulation. Annals of the New York Academy of Sciences, 1251, E1E24. doi:10.1111/j.1749-6632.2012.06751.xGoogle Scholar
Pagliaccio, D., Luby, J. L., Bogdan, R., Agrawal, A., Gaffrey, M. S., Belden, A. C., … Barch, D. M. (2015). Amygdala functional connectivity, HPA axis genetic variation, and life stress in children and relations to anxiety and emotion regulation. Journal of Abnormal Psychology, 124, 817833. doi:10.1037/abn0000094Google Scholar
Price, R. B., Kuckertz, J. M., Siegle, G. J., Ladouceur, C. D., Silk, J. S., Ryan, N. D., … Amir, N. (2015). Empirical recommendations for improving the stability of the dot-probe task in clinical research. Psychological Assessment, 27, 365376. doi:10.1037/pas0000036Google Scholar
Rhee, S. H., Lahey, B. B., & Waldman, I. D. (2015). Comorbidity among dimensions of childhood psychopathology: Converging evidence from behavior genetics. Child Development Perspectives, 9, 2631. doi:10.1111/cdep.12102Google Scholar
Tone, E. B., Garn, C. L., & Pine, D. S. (2016). Anxiety regulation: A developmental psychopathology perspective. In Cicchetti, D. (Ed.), Developmental psychopathology: Vol. 2. Developmental neuroscience (3rd ed., pp. 523556). Hoboken, NJ: Wiley.Google Scholar
Troller-Renfree, S., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2016). Deficits in error monitoring are associated with externalizing but not internalizing behaviors among children with a history of institutionalization. Journal of Child Psychology and Psychiatry, 57, 11451153. doi:10.1111/jcpp.12604Google Scholar
Venables, N. C., Foell, J., Yancey, J. R., Kane, M. J., Engle, R. W., & Patrick, C. J. (2018). Quantifying inhibitory control as externalizing proneness: A cross-domain model. Advance online pubication. Clinical Psychological Science.Google Scholar
Weinberg, A., Meyer, A., Hale-Rude, E., Perlman, G., Kotov, R., Klein, D. N., & Hajcak, G. (2016). Error-related negativity (ERN) and sustained threat: Conceptual framework and empirical evaluation in an adolescent sample. Psychophysiology, 53, 372385. doi:10.1111/psyp.12538Google Scholar
White, L. K., Moore, T. M., Calkins, M. E., Wolf, D. H., Satterthwaite, T. D., Leibenluft, E., … Gur, R. E. (2017). An evaluation of the specificity of executive function impairment in developmental psychopathology. Journal of the American Academy of Child & Adolescent Psychiatry, 56, 975982. doi:10.1016/j.jaac.2017.08.016Google Scholar
White, L. K., Sequeira, S., Britton, J. C., Brotman, M. A., Gold, A. L., Berman, E., … Pine, D. S. (2017). Complementary features of attention bias modification therapy and cognitive-behavioral therapy in pediatric anxiety disorders. American Jorunal of Psychiatry, 174, 775784. doi:10.1176/appi.ajp.2017.16070847Google Scholar