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Tuning of brain–autonomic coupling by prior threat exposure: Implications for internalizing problems in Mexican-origin adolescents

Published online by Cambridge University Press:  14 May 2019

David G. Weissman ,
Amanda E. Guyer ,
Emilio Ferrer ,
Richard W. Robins  and
Paul D. Hastings
David G. Weissman*
Affiliation:
Department of Psychology, Harvard University, Cambridge, MA, USA Center for Mind and Brain, University of California–Davis, Davis, CA, USA Department of Psychology, University of California–Davis, Davis, CA, USA
Amanda E. Guyer
Affiliation:
Center for Mind and Brain, University of California–Davis, Davis, CA, USA Department of Human Ecology, University of California–Davis, Davis, CA, USA
Emilio Ferrer
Affiliation:
Department of Psychology, University of California–Davis, Davis, CA, USA
Richard W. Robins
Affiliation:
Department of Psychology, University of California–Davis, Davis, CA, USA
Paul D. Hastings
Affiliation:
Center for Mind and Brain, University of California–Davis, Davis, CA, USA Department of Psychology, University of California–Davis, Davis, CA, USA
*
Author for Correspondence: David G. Weissman, Department of Psychology, Harvard University, William James Hall, 33 Kirkland Street, Cambridge, MA 02138; E-mail: dweissman@fas.harvard.edu.
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Abstract

Exposure to threat increases the risk for internalizing problems in adolescence. Deficits in integrating bodily cues into representations of emotion are thought to contribute to internalizing problems. Given the role of the medial prefrontal cortex in regulating bodily responses and integrating them into representations of emotional states, coordination between activity in the medial prefrontal cortex and autonomic nervous system responses may be influenced by past threat exposure with consequences for the emergence of internalizing problems. A sample of 179 Mexican-origin adolescents (88 female) reported on neighborhood and school crime, peer victimization, and discrimination when they were 10–16 years old. At age 17, participants underwent a functional neuroimaging scan during which they viewed pictures of emotional faces while respiratory sinus arrhythmia (RSA) and skin conductance responses were measured. Adolescents also reported symptoms of internalizing problems. Greater exposure to threats across adolescence was associated with more internalizing problems. Threat exposure was also associated with stronger negative coupling between the ventromedial prefrontal cortex and RSA. Stronger negative ventromedial prefrontal cortex–RSA coupling was associated with fewer internalizing problems. These results suggest the degree of coordinated activity between the brain and parasympathetic nervous system is both enhanced by threat experiences and decreased in adolescents with more internalizing problems.

Keywords

adversitycommunity crimediscriminationfunctional magnetic resonance imagingpeer victimizationphysiology

Information

Type
Special Issue Articles
Information
Development and Psychopathology , Volume 31 , Special Issue 3: Emotion Dysregulation and Emerging Psychopathology , August 2019 , pp. 1127 - 1141
Copyright
Copyright © Cambridge University Press 2019 

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References

Arnett, J. J. (1999). Adolescent storm and stress, reconsidered. American Psychologist, 54, 317–326. doi:10.1037/0003-066X.54.5.317Google Scholar
Barrett, L. F., & Simmons, W. K. (2015). Interoceptive predictions in the brain. Nature Reviews Neuroscience, 16, 409–419. doi:10.1038/nrn3950Google Scholar
Beauchaine, T. P. (2001). Vagal tone, development, and Gray's motivational theory: Toward an integrated model of autonomie nervous system functioning in psychopathology. Development and Psychopathology, 13, 183–214. doi:10.1017/S0954579401002012Google Scholar
Beauchaine, T. P. (2015a). Future directions in emotion dysregulation and youth psychopathology. Journal of Clinical Child and Adolescent Psychology, 44, 875–896. doi:10.1080/15374416.2015.1038827Google Scholar
Beauchaine, T. P. (2015b). Respiratory sinus arrhythmia: A transdiagnostic biomarker of emotion dysregulation and psychopathology. Current Opinion in Psychology, 1, 43–47. doi:10.1016/j.copsyc.2015.01.017Google Scholar
Beauchaine, T. P., Bell, Z., Knapton, E., McDonough-Caplan, H., Shader, T., & Zisner, A. (2019). Respiratory sinus arrhythmia reactivity across empirically based structural dimensions of psychopathology: A meta-analysis. Psychophysiology, e13329. doi:10.1111/psyp.13329Google 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, 108–118. doi:10.1016/j.ijpsycho.2016.12.014Google Scholar
Beissner, F., Meissner, K., Bar, K.-J., & Napadow, V. (2013). The autonomic brain: An activation likelihood estimation meta-analysis for central processing of autonomic function. Journal of Neuroscience, 19, 10503–10511. doi:10.1523/JNEUROSCI.1103-13.2013Google Scholar
Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1991). Autonomic determinism: The modes of autonomic control, the doctrine of autonomic space, and the laws of autonomic constraint. Psychological Review, 98, 459–487. doi:10.1037/0033-295X.98.4.459Google Scholar
Berntson, G. G., Thomas Bigger, J., Eckberg, D. L., Grossman, P., Kaufmann, P. G., Malik, M., … Van Der Molen, M. W. (1997). Heart rate variability: Origins methods, and interpretive caveats. Psychophysiology, 34, 623–648. doi:10.1111/j.1469-8986.1997.tb02140.xGoogle Scholar
Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., & Neer, S. M. K. (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, 545–553. doi:10.1097/00004583-199704000-00018Google Scholar
Blair, C., & Raver, C. C. (2012). Child development in the context of adversity: Experiential canalization of brain and behavior. American Psychologist, 67, 309–318. doi:10.1037/a0027493Google Scholar
Blakemore, S.-J., & Mills, K. L. (2014). Is adolescence a sensitive period for sociocultural processing? Annual Review of Psychology, 65, 187–207. doi:10.1146/annurev-psych-010213-115202Google Scholar
Bowen, N. K., & Bowen, G. L. (1999). Effects of crime and violence in neighborhoods and schools on the school behavior and performance of adolescents. Journal of Adolescent Research, 14, 319–342. doi:10.1177/0743558499143003Google Scholar
Braithwaite, J., Watson, D., Robert, J., & Mickey, R. (2013). A guide for Analysing Electrodermal Activity (EDA) & Skin Conductance Responses (SCRs) for psychological experiments (Vol. 49). Cambridge: Cambridge University Press.Google Scholar
Brown, B. B., & Larson, J. (2009). Peer relationships in adolescence. In Lerner, R. M. & Steinberg, L. (Eds.), Handbook of adolescent psychology (pp. 74–103). Hoboken, NJ: Wiley.Google Scholar
Bylsma, L. M., Salomon, K., Taylor-Clift, A., Morris, B. H., & Rottenberg, J. (2014). Respiratory sinus arrhythmia reactivity in current and remitted major depressive disorder. Psychosomatic Medicine, 76, 66–73. doi:10.1097/PSY.0000000000000019Google Scholar
Carnevali, L., Mancini, M., Koenig, J., Makovac, E., Watson, D. R., Meeten, F., … Ottaviani, C. (2019). Cortical morphometric predictors of autonomic dysfunction in generalized anxiety disorder. Autonomic Neuroscience, 217, 41–48. doi:10.1016/J.AUTNEU.2019.01.001Google Scholar
Casement, M. D., 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. doi:10.1016/j.dcn.2013.12.003Google Scholar
Chen, G., Saad, Z. S., Britton, J. C., Pine, D. S., & Cox, R. W. (2013). Linear mixed-effects modeling approach to FMRI group analysis. NeuroImage, 73, 176–190. doi:10.1016/J.NEUROIMAGE.2013.01.047Google Scholar
Chida, Y., & Hamer, M. (2008). Chronic psychosocial factors and acute physiological responses to laboratory-induced stress in healthy populations: A quantitative review of 30 years of investigations. Psychological Bulletin, 134, 829–885. doi:10.1037/a0013342Google Scholar
Cicchetti, D., & Curtis, W. J. (2005). An event-related potential study of the processing of affective facial expressions in young children who experienced maltreatment during the first year of life. Development and Psychopathology, 17, 641–677. doi:10.1017/S0954579405050315Google Scholar
Cicchetti, D., & Toth, S. L. (2005). Child maltreatment. Annual Review of Clinical Psychology 1, 409–438. doi:10.1146/annurev.clinpsy.1.102803.144029Google 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 (pp. 346–386). Hoboken, NJ: Wiley.Google Scholar
Colich, N. L., Williams, E. S., Ho, T. C., King, L. S., Humphreys, K. L., Price, A. N., … Gotlib, I. H. (2017). The association between early life stress and prefrontal cortex activation during implicit emotion regulation is moderated by sex in early adolescence. Development and Psychopathology, 29, 1851–1864. doi:10.1017/S0954579417001444Google Scholar
Cook, C. R., Williams, K. R., Guerra, N. G., Kim, T. E., & Sadek, S. (2010). Predictors of bullying and victimization in childhood and adolescence: A meta-analytic investigation. School Psychology Quarterly, 25, 65–83. doi:10.1037/a0020149Google Scholar
Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173. doi:10.1006/cbmr.1996.0014Google Scholar
Cox, R. W., Chen, G., Glen, D. R., Reynolds, R. C., & Taylor, P. A. (2017). fMRI clustering and false-positive rates. Proceedings of the National Academy of Sciences of the USA, 114, E3370–E3371. doi:10.1073/pnas.1614961114Google Scholar
Critchley, H. D. (2005). Neural mechanisms of autonomic, affective, and cognitive integration. Journal of Comparative Neurology, 493, 154–166. doi:10.1002/cne.20749Google Scholar
Critchley, H. D. (2009). Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. International Journal of Psychophysiology, 73, 88–94. doi:10.1016/j.ijpsycho.2009.01.012Google Scholar
Csikszentmihalyi, M., Larson, R., & Prescott, S. (2014). The ecology of adolescent activity and experience. In Applications of flow in human development and education: The collected works of Mihaly Csikszentmihalyi (Vol. 6, pp. 241–254). New York: Kluwer Academic.Google Scholar
Dawson, M. E., Schell, A. M., & Filion, D. L. (2016). The electrodermal system. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.), Handbook of Psychophysiology. 217–243. Cambridge: Cambridge University Press.Google Scholar
Delgado, M. Y., Updegraff, K. A., Roosa, M. W., & Umaña-Taylor, A. J. (2011). Discrimination and Mexican-origin adolescents’ adjustment: The moderating roles of adolescents’, mothers’, and fathers’ cultural orientations and values. Journal of Youth and Adolescence, 40, 125–139. doi:10.1007/s10964-009-9467-zGoogle Scholar
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011). The adaptive calibration model of stress responsivity. Neuroscience & Biobehavioral Reviews, 35, 1562–1592. doi:10.1016/j.neubiorev.2010.11.007Google Scholar
De Morree, H. M., Rutten, G. J., Szabo, B. M., Sitskoorn, M. M., & Kop, W. J. (2016). Effects of insula resection on autonomic nervous system activity. Journal of Neurosurgical Anesthesiology, 28, 153–158. doi:10.1097/ANA.0000000000000207Google Scholar
Dodge, K. A., Pettit, G. S., Bates, J. E., & Valente, E. (1995). Social information-processing patterns partially mediate the effect of early physical abuse on later conduct problems. Journal of Abnormal Psychology, 104, 832–843. doi:10.1037/0021-843X.104.4.632Google Scholar
Edwards, V. J., Holden, G. W., Felitti, V. J., & Anda, R. F. (2003). Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: Results from the adverse childhood experiences study. American Journal of Psychiatry, 160, 1453–1460. doi:10.1176/appi.ajp.160.8.1453Google Scholar
El-Sheikh, M. (2005). Stability of respiratory sinus arrhythmia in children and young adolescents: A longitudinal examination. Developmental Psychobiology, 46, 66–74. doi:10.1002/dev.20036Google Scholar
Espinoza, G., Gonzales, N. A., & Fuligni, A. J. (2013). Daily school peer victimization experiences among Mexican-American adolescents: Associations with psychosocial, physical and school adjustment. Journal of Youth and Adolescence, 42, 1775–1788. doi:10.1007/s10964-012-9874-4Google Scholar
Evans, G. W., Li, D., & Whipple, S. S. (2013). Cumulative risk and child development. Psychological Bulletin, 139, 1342–1396. doi:10.1037/a0031808Google Scholar
Evans, G. W., Swain, J. E., King, A. P., Wang, X., Javanbakht, A., Ho, S. S., … Liberzon, I. (2016). Childhood cumulative risk exposure and adult amygdala volume and function. Journal of Neuroscience Research, 94, 535–543. doi:10.1002/jnr.23681Google Scholar
Fowler, P. J., Tompsett, C. J., Braciszewski, J. M., Jacques-Tiura, A. J., & Baltes, B. B. (2009). Community violence: A meta-analysis on the effect of exposure and mental health outcomes of children and adolescents. Development and Psychopathology, 21, 227–259. doi:10.1017/S0954579409000145Google Scholar
Frankenhuis, W. E., & de Weerth, C. (2013). Does early-life exposure to stress shape or impair cognition? Current Directions in Psychological Science, 22, 407–412. doi:10.1177/0963721413484324Google Scholar
Gabard-Durnam, L. J., Flannery, J., Goff, B., Gee, D. G., Humphreys, K. L., Telzer, E., … Tottenham, N. (2014). The development of human amygdala functional connectivity at rest from 4 to 23 years: A cross-sectional study. NeuroImage, 95, 193–207. doi:10.1016/j.neuroimage.2014.03.038Google Scholar
Ganzel, B. L., Morris, P. A., & Wethington, E. (2010). Allostasis and the human brain: Integrating models of stress from the social and life sciences. Psychological Review, 117, 134–177. doi:10.1037/a0017773Google Scholar
Gee, D. G., Gabard-Durnam, L. J., Flannery, J., Goff, B., Humphreys, K. L., Telzer, E. H., … Tottenham, N. (2013). Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation. Proceedings of the National Academy of Sciences of the USA, 110, 15638–15643. doi:10.1073/pnas.1307893110Google Scholar
Gee, D. G., Humphreys, K. L., Flannery, J., Goff, B., Telzer, E. H., Shapiro, M., … Tottenham, N. (2013). A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. Journal of Neuroscience, 33, 4584–4593. doi:10.1523/JNEUROSCI.3446-12.2013Google Scholar
Gianaros, P. J., Van der Veen, F. M., & Jennings, J. R. (2004). Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: Implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology, 41, 521–530. doi:10.1111/1469-8986.2004.00179.xGoogle Scholar
Grossman, P., & Taylor, E. W. (2007). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology, 74, 263–285. doi:10.1016/J.BIOPSYCHO.2005.11.014Google Scholar
Guyer, A. E., Choate, V. R., Grimm, K. J., Pine, D. S., & Keenan, K. (2011). Emerging depression is associated with face memory deficits in adolescent girls. Journal of the American Academy of Child & Adolescent Psychiatry, 50, 180–190. doi:10.1016/j.jaac.2010.11.008Google Scholar
Guyer, A. E., Kaufman, J., Hodgdon, H. B., Masten, C. L., Jazbec, S., Pine, D. S., & Ernst, M. (2006). Behavioral alterations in reward system function: The role of childhood maltreatment and psychopathology. Journal of the American Academy of Child & Adolescent Psychiatry, 45, 1559–1567. doi:10.1097/01.chi.0000227882.50404.11Google Scholar
Guyer, A. E., Silk, J. S., & Nelson, E. E. (2016). The neurobiology of the emotional adolescent: From the inside out. Neuroscience & Biobehavioral Reviews, 70, 74–85. doi:10.1016/j.neubiorev.2016.07.037Google Scholar
Hanson, J. L., Knodt, A. R., Brigidi, B. D., & Hariri, A. R. (2015). Lower structural integrity of the uncinate fasciculus is associated with a history of child maltreatment and future psychological vulnerability to stress. Development and Psychopathology, 27(4, Pt. 2), 1611–1619. doi:10.1017/S0954579415000978Google Scholar
Hartung, C. M., & Widiger, T. A. (1998). Gender differences in the diagnosis of mental disorders: Conclusions and controversies of the DSM-IV. Psychological Bulletin, 123, 260–278. doi:10.1037/0033-2909.123.3.260Google Scholar
Hastings, P. D., & Kahle, S. (in press). Get bent into shape: The non-linear, multi-system, contextually-embedded psychophysiology of emotional development. In LoBue, V., Perez-Edgar, K., & Buss, K. A. (Eds.), Handbook of emotional development. New York: Springer.Google Scholar
Hastings, P. D., Kahle, S. S., & Han, G. H.-P. (2014). Developmental affective psychophysiology: Using physiology to inform our understanding of emotional development. Contributions to Human Development, 26, 13–28. doi:10.1159/000354347Google Scholar
Hastings, P. D., Kahle, S., & Nuselovici, J. (2014). How well socially wary preschoolers fare over time depends on their parasympathetic regulation and socialization. Child Development, 85, 1586–1600. doi:10.1111/cdev.12228Google Scholar
Hastings, P. D., Klimes-Dougan, B., Kendziora, K. T., Brand, A., & Zahn-Waxler, C. (2014). Regulating sadness and fear from outside and within: Mothers’ emotion socialization and adolescents’ parasympathetic regulation predict the development of internalizing difficulties. Development and Psychopathology, 26, 1369–1384. doi:10.1017/S0954579414001084Google Scholar
Hastings, P. D., Sullivan, C., McShane, K. E., Coplan, R. J., Utendale, W. T., & Vyncke, J. D. (2008). Parental socialization, vagal regulation, and preschoolers’ anxious difficulties: Direct mothers and moderated fathers. Child Development, 79, 45–64. doi:10.1111/j.1467-8624.2007.01110.xGoogle Scholar
Hein, T. C., & Monk, C. S. (2017). Research Review: Neural response to threat in children, adolescents, and adults after child maltreatment—A quantitative meta-analysis. Journal of Child Psychology and Psychiatry and Allied Disciplines, 58, 222–230. doi:10.1111/jcpp.12651Google Scholar
Heleniak, C., Jenness, J. L., Vander Stoep, A., McCauley, E., & McLaughlin, K. A. (2016). Childhood maltreatment exposure and disruptions in emotion regulation: A transdiagnostic pathway to adolescent internalizing and externalizing psychopathology. Cognitive Therapy and Research, 40, 394–415. doi:10.1007/s10608-015-9735-zGoogle Scholar
Heleniak, C., King, K. M., Monahan, K. C., & McLaughlin, K. A. (2018). Disruptions in emotion regulation as a mechanism linking community violence exposure to adolescent internalizing problems. Journal of Research on Adolescence, 28, 229–244. doi:10.1111/jora.12328Google Scholar
Heller, A. S., Cohen, A. O., Dreyfuss, M. F. W., & Casey, B. J. (2016). Changes in cortico-subcortical and subcortico-subcortical connectivity impact cognitive control to emotional cues across development. Social Cognitive and Affective Neuroscience, 11, 1910–1918. doi:10.1093/scan/nsw097Google Scholar
Helm, J. L., Miller, J. G., Kahle, S., Troxel, N. R., & Hastings, P. D. (2018). On measuring and modeling physiological synchrony in dyads. Multivariate Behavioral Research, 53, 521–543. doi:10.1080/00273171.2018.1459292Google Scholar
Herringa, R. J., Birn, R. M., Ruttle, P. L., Burghy, C. A., Stodola, D. E., Davidson, R. J., & Essex, M. J. (2013). Childhood maltreatment is associated with altered fear circuitry and increased internalizing symptoms by late adolescence. Proceedings of the National Academy of Sciences USA, 110, 19119–19124. doi:10.1073/pnas.1310766110Google Scholar
Herringa, R. J., Burghy, C. A., Stodola, D. E., Fox, M. E., Davidson, R. J., & Essex, M. J. (2016). Enhanced prefrontal-amygdala connectivity following childhood adversity as a protective mechanism against internalizing in adolescence. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 1, 326–334. doi:10.1016/J.BPSC.2016.03.003Google Scholar
Jedd, K., Hunt, R. H., Cicchetti, D., Hunt, E., Cowell, R. A., Rogosch, F. A., … Thomas, K. M. (2015). Long-term consequences of childhood maltreatment: Altered amygdala functional connectivity. Development and Psychopathology, 27, 1577–1589. doi:10.1017/S0954579415000954Google Scholar
Jenness, J. L., Miller, A. B., Rosen, M. L., & McLaughlin, K. A. (2018). Extinction learning as a potential mechanism linking high vagal tone with lower PTSD symptoms among abused youth. Journal of Abnormal Child Psychology, 46, 659–670. doi:10.1007/s10802-018-0464-0Google Scholar
Kelsey, R. M. (1991). Electrodermal lability and myocardial reactivity to stress. Psychophysiology, 28, 619–631. doi:10.1111/j.1469-8986.1991.tb01005.xGoogle Scholar
Kemp, A. H., Brunoni, A. R., Santos, I. S., Nunes, M. A., Dantas, E. M., De Figueiredo, R. C., … Lotufo, P. A. (2014). Effects of depression, anxiety, comorbidity, and antidepressants on resting-state heart rate and its variability: An ELSA-Brasil cohort baseline study. American Journal of Psychiatry, 171, 1328–1334. doi:10.1176/appi.ajp.2014.13121605Google Scholar
Kessler, R. C., McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., … Williams, D. R. (2010). Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. British Journal of Psychiatry, 197, 378–385. doi:10.1192/bjp.bp.110.080499Google Scholar
Kessler, R. C., Mickelson, K. D., & Williams, D. R. (1999). The prevalence, distribution, and mental health correlates of perceived discrimination in the United States. Journal of Health and Social Behavior, 40, 208. doi:10.2307/2676349Google Scholar
Kim, J., & Cicchetti, D. (2010). Longitudinal pathways linking child maltreatment, emotion regulation, peer relations, and psychopathology. Journal of Child Psychology and Psychiatry and Allied Disciplines, 51, 706–716. doi:10.1111/j.1469-7610.2009.02202.xGoogle Scholar
Koenig, J., Kemp, A. H., Beauchaine, T. P., Thayer, J. F., & Kaess, M. (2016). Depression and resting state heart rate variability in children and adolescents—A systematic review and meta-analysis. Clinical Psychology Review, 46, 136–150. doi:10.1016/j.cpr.2016.04.013Google Scholar
Koenig, J., & Thayer, J. F. (2016). Sex differences in healthy human heart rate variability: A meta-analysis. Neuroscience & Biobehavioral Reviews, 64, 288–310. doi:10.1016/J.NEUBIOREV.2016.03.007Google Scholar
Koenig, J., Westlund Schreiner, M., Klimes-Dougan, B., Ubani, B., Mueller, B., Kaess, M., & Cullen, K. R. (2018). Brain structural thickness and resting state autonomic function in adolescents with major depression. Social Cognitive and Affective Neuroscience, 13, 741–753. doi:10.1093/scan/nsy046Google Scholar
Koenig, J., Westlund Schreiner, M., Klimes-Dougan, B., Ubani, B., Mueller, B. A., Lim, K. O., … Cullen, K. R. (2018). Increases in orbitofrontal cortex thickness following antidepressant treatment are associated with changes in resting state autonomic function in adolescents with major depression—Preliminary findings from a pilot study. Psychiatry Research: Neuroimaging, 281, 35–42. doi:10.1016/J.PSCYCHRESNS.2018.08.013Google Scholar
Kovacs, M. (2011). Children's Depression Inventory (CDI2). North Tonawanda, NY: Multi-Health Systems.Google Scholar
Lane, R. D., McRae, K., Reiman, E. M., Chen, K., Ahern, G. L., & Thayer, J. F. (2009). Neural correlates of heart rate variability during emotion. NeuroImage, 44, 213–222. doi:10.1016/J.NEUROIMAGE.2008.07.056Google Scholar
Larson, R. W., Moneta, G., Richards, M. H., & Wilson, S. (2002). Continuity, stability, and change in daily emotional experience across adolescence. Child Development, 73, 1151–1165. doi:10.1111/1467-8624.00464Google Scholar
Lissek, S., Powers, A. S., McClure, E. B., Phelps, E. A., Woldehawariat, G., Grillon, C., & Pine, D. S. (2005). Classical fear conditioning in the anxiety disorders: A meta-analysis. Behaviour Research and Therapy, 43, 1391–1424. doi:10.1016/j.brat.2004.10.007Google Scholar
MacKinnon, D. P., Krull, J. L., & Lockwood, C. M. (2000). Equivalence of the mediation, confounding and suppression effect. Prevention Science, 1, 173–181. doi:10.1023/A1026595011371Google Scholar
Maheu, F. S., Dozier, M., Guyer, A. E., Mandell, D., Peloso, E., Poeth, K., … Ernst, M. (2010). A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect. Cognitive, Affective and Behavioral Neuroscience, 10, 34–49. doi:10.3758/CABN.10.1.34Google Scholar
Masten, C. L., Guyer, A. E., Hodgdon, H. B., McClure, E. B., Charney, D. S., Ernst, M., … Monk, C. S. (2008). Recognition of facial emotions among maltreated children with high rates of post-traumatic stress disorder. Child Abuse and Neglect, 32, 139–153. doi:10.1016/j.chiabu.2007.09.006Google Scholar
Maughan, A., & Cicchetti, D. (2002). Impact of child maltreatment and interadult violence on children's emotion regulation abilities and socioemotional adjustment. Child Development, 73, 1525–1542. doi:10.1111/1467-8624.00488Google Scholar
McCrory, E., De Brito, S. A., & Viding, E. (2010). Research Review: The neurobiology and genetics of maltreatment and adversity. Journal of Child Psychology and Psychiatry and Allied Disciplines, 51, 1079–1095. doi:10.1111/j.1469-7610.2010.02271.xGoogle Scholar
McEwen, B. S., & Seeman, T. (1999). Protective and damaging effects of mediators of stress. Elaborating and testing the concepts of allostasis and allostatic load. Annals of the New York Academy of Sciences, 896, 30–47. doi:10.1111/j.1749-6632.1999.tb08103.xGoogle Scholar
McLaughlin, K. A., Alves, S., & Sheridan, M. A. (2014). Vagal regulation and internalizing psychopathology among adolescents exposed to childhood adversity. Developmental Psychobiology, 56, 1036–1051. doi:10.1002/dev.21187Google Scholar
McLaughlin, K. A., Hatzenbuehler, M. L., & Hilt, L. M. (2009). Emotion dysregulation as a mechanism linking peer victimization to internalizing symptoms in adolescents. Journal of Consulting and Clinical Psychology, 77, 894–904. doi:10.1037/a0015760Google Scholar
McLaughlin, K. A., Rith-Najarian, L., Dirks, M. A., & Sheridan, M. A. (2015). Low vagal tone magnifies the association between psychosocial stress exposure and internalizing psychopathology in adolescents. Journal of Clinical Child and Adolescent Psychology, 44, 314–328. doi:10.1080/15374416.2013.843464Google Scholar
McLaughlin, K. A., & Sheridan, M. A. (2016). Beyond cumulative risk: A dimensional approach to childhood adversity. Current Directions in Psychological Science, 25, 239–245. doi:10.1177/0963721416655883Google Scholar
McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014). Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience. Neuroscience and Biobehavioral Reviews, 47, 578–591. doi:10.1016/j.neubiorev.2014.10.012Google Scholar
Merri, M., Farden, D. C., Mottley, J. G., & Titlebaum, E. L. (1990). Sampling frequency of the electrocardiogram for spectral analysis of the heart rate variability. IEEE Transactions on Biomedical Engineering, 37, 99–106. doi:10.1109/10.43621Google Scholar
Miller, A. B., Sheridan, M. A., Hanson, J. L., McLaughlin, K. A., Bates, J. E., Lansford, J. E., … Dodge, K. A. (2018). Dimensions of deprivation and threat, psychopathology, and potential mediators: A multi-year longitudinal analysis. Journal of Abnormal Psychology, 127, 160–170. doi:10.1037/abn0000331Google Scholar
Monahan, K. C., Guyer, A. E., Silk, J., Fitzwater, T., & Steinberg, L. (2016). Integration of developmental neuroscience and contextual approaches to the study of adolescent psychopathology. In Cicchetti, D. (Ed.), Developmental psychopathology. Hoboken, NJ: Wiley.Google Scholar
Mrug, S., & Windle, M. (2010). Prospective effects of violence exposure across multiple contexts on early adolescents’ internalizing and externalizing problems. Journal of Child Psychology and Psychiatry and Allied Disciplines, 51, 951–963. doi:10.1111/j.1469-7610.2010.02222.xGoogle Scholar
Muehsam, D., Lutgendorf, S., Mills, P. J., Rickhi, B., Chevalier, G., Bat, N., … Gurfein, B. (2017). The embodied mind: A review on functional genomic and neurological correlates of mind-body therapies. Neuroscience & Biobehavioral Reviews, 73, 165–181. doi:10.1016/J.NEUBIOREV.2016.12.027Google Scholar
Muthén, L., & Muthén, B. (2017). Mplus user's guide (8th ed.). Los Angeles: Author.Google Scholar
Nagai, Y., Critchley, H., Featherstone, E., Trimble, M., & Dolan, R. (2004). Activity in ventromedial prefrontal cortex covaries with sympathetic skin conductance level: A physiological account of a “default mode” of brain function. NeuroImage, 22, 243–251. doi:10.1016/j.neuroimage.2004.01.019Google Scholar
Nelson, E. E., Jarcho, J. M., & Guyer, A. E. (2016). Social re-orientation and brain development: An expanded and updated view. Developmental Cognitive Neuroscience, 17, 118–127. doi:10.1016/j.dcn.2015.12.008Google Scholar
Nikula, R. (1991). Psychological correlates of nonspecific skin conductance responses. Psychophysiology, 28, 86–90. doi:10.1111/j.1469-8986.1991.tb03392.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 HHS Public Access. Journal of Abnormal Psychology, 124, 817–833. doi:10.1037/abn0000094Google Scholar
Park, A. T., Leonard, J. A., Saxler, P. K., Cyr, A. B., Gabrieli, J. D. E., & Mackey, A. P. (2018). Amygdala–medial prefrontal cortex connectivity relates to stress and mental health in early childhood. Social Cognitive and Affective Neuroscience, 13, 430–439. doi:10.1093/scan/nsy017Google Scholar
Pattwell, S. S., Liston, C., Jing, D., Ninan, I., Yang, R. R., Witztum, J., … Lee, F. S. (2016). Dynamic changes in neural circuitry during adolescence are associated with persistent attenuation of fear memories. Nature Communications, 7, 11475. doi:10.1038/ncomms11475Google Scholar
Paulus, M. P., & Stein, M. B. (2010). Interoception in anxiety and depression. Brain Structure & Function, 214, 451–463. doi:10.1007/s00429-010-0258-9Google Scholar
Pollak, S. D. (2003). Experience-dependent affective learning and risk for psychopathology in children. Annals of the New York Academy of Sciences, 1008, 102–111. doi:10.1196/annals.1301.011Google Scholar
Pollak, S. D., Cicchetti, D., Hornung, K., & Reed, A. (2000). Recognizing emotion in faces: Developmental effects of child abuse and neglect. Developmental Psychology, 36, 679–688. doi:10.1037/0012-1649.36.5.679Google Scholar
Pollak, S. D., & Kistler, D. J. (2002). Early experience is associated with the development of categorical representations for facial expressions of emotion. Proceedings of the National Academy of Sciences, 99, 9072–9076. doi:10.1073/pnas.142165999Google Scholar
Pollak, S. D., & Sinha, P. (2002). Effects of early experience on children's recognition of facial displays of emotion. Developmental Psychology, 38, 784–791. doi:10.1037/0012-1649.38.5.784Google Scholar
Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74, 116–143. doi:10.1016/j.biopsycho.2006.06.009Google Scholar
Porges, S. W. (2009). The polyvagal theory: New insights into adaptive reactions of the autonomic nervous system. Cleveland Clinic Journal of Medicine, 76(Suppl. 2), S86–S90. doi:10.3949/ccjm.76.s2.17Google Scholar
Porges, S. W., Doussard-Roosevelt, J. A., & Maiti, A. K. (1994). Vagal tone and the physiological regulation of emotion. Monographs of the Society for Research in Child Development, 59 167. doi:10.1111/j.1540-5834.1994.tb01283.xGoogle Scholar
Prinstein, M. J., Cheah, C. S. L., & Guyer, A. E. (2005). Peer victimization, cue interpretation, and internalizing symptoms: Preliminary concurrent and longitudinal findings for children and adolescents. Journal of Clinical Child and Adolescent Psychology, 34, 11–24. doi:10.1207/s15374424jccp3401_2Google Scholar
Quadt, L., Critchley, H. D., & Garfinkel, S. N. (2019). Interoception and emotion: Shared mechanisms and clinical implications. In Tsakiris, M. & De Preester, H. (Eds.), The interoceptive mind: From homeostasis to awareness (1st ed., pp. 123–143). Oxford: Oxford University Press.Google Scholar
Reijntjes, A., Kamphuis, J. H., Prinzie, P., & Telch, M. J. (2010). Peer victimization and internalizing problems in children: A meta-analysis of longitudinal studies. Child Abuse and Neglect, 34, 244–252. doi:10.1016/j.chiabu.2009.07.009Google Scholar
Riniolo, T., & Porges, S. W. (1997). Inferential and descriptive influences on measures of respiratory sinus arrhythmia: Sampling rate, R-wave trigger accuracy, and variance estimates. Psychophysiology, 34, 613–621. doi:10.1111/j.1469-8986.1997.tb01748.xGoogle Scholar
Ritz, T. (2009). Studying noninvasive indices of vagal control: The need for respiratory control and the problem of target specificity. Biological Psychology, 80, 158–168. doi:10.1016/j.biopsycho.2008.08.003Google Scholar
Rottenberg, J. (2007). Cardiac vagal control in depression: A critical analysis. Biological Psychology, 74, 200–211. doi:10.1016/j.biopsycho.2005.08.010Google Scholar
Rottenberg, J., Clift, A., Bolden, S., & Salomon, K. (2007). RSA fluctuation in major depressive disorder. Psychophysiology, 44, 450–458. doi:10.1111/j.1469-8986.2007.00509.xGoogle Scholar
Schriber, R. A., & Guyer, A. E. (2016). Adolescent neurobiological susceptibility to social context. Developmental Cognitive Neuroscience, 19, 1–18. doi:10.1016/j.dcn.2015.12.009Google Scholar
Seaton, E. K., Neblett, E. W., Cole, D. J., & Prinstein, M. J. (2013). Perceived discrimination and peer victimization among African American and Latino youth. Journal of Youth and Adolescence, 42, 342–350. doi:10.1007/s10964-012-9848-6Google Scholar
Sequeira, H., Hot, P., Silvert, L., & Delplanque, S. (2009). Electrical autonomic correlates of emotion. International Journal of Psychophysiology, 71, 50–56. doi:10.1016/j.ijpsycho.2008.07.009Google Scholar
Seth, A. K., & Friston, K. J. (2016). Active interoceptive inference and the emotional brain. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 2060007. doi:10.1098/rstb.2016.0007Google Scholar
Shader, T. M., Gatzke-Kopp, L. M., Crowell, S. E., Jamila Reid, M., Thayer, J. F., Vasey, M. W., … Beauchaine, T. P. (2018). Quantifying respiratory sinus arrhythmia: Effects of misspecifying breathing frequencies across development. Development and Psychopathology, 30, 351–366. doi:10.1017/S0954579417000669Google Scholar
Shaffer, D., Fisher, P., Lucas, C. P., Dulcan, M. K., & Schwab-Stone, M. E. (2000). NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): Description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry, 39, 28–38. doi:10.1097/00004583-200001000-00014Google Scholar
Shahrestani, S., Stewart, E. M., Quintana, D. S., Hickie, I. B., & Guastella, A. J. (2015). Heart rate variability during adolescent and adult social interactions: A meta-analysis. Biological Psychology, 105, 43–50. doi:10.1016/j.biopsycho.2014.12.012Google Scholar
Sharp, C., Goodyer, I. M., & Croudace, T. J. (2006). The Short Mood and Feelings Questionnaire (SMFQ): A unidimensional item response theory and categorical data factor analysis of self-report ratings from a community sample of 7- through 11-year-old children. Journal of Abnormal Child Psychology, 34, 379–391. doi:10.1007/s10802-006-9027-xGoogle Scholar
Sheppard, C. S., Giletta, M., & Prinstein, M. J. (2016). Peer victimization trajectories at the adolescent transition: Associations among chronic victimization, peer-reported status, and adjustment. Journal of Clinical Child and Adolescent Psychology, 48, 218–227. doi:10.1080/15374416.2016.1261713Google Scholar
Sheridan, M. A., & McLaughlin, K. A. (2014). Dimensions of early experience and neural development: Deprivation and threat. Trends in Cognitive Sciences, 18, 580–585. doi:10.1016/j.tics.2014.09.001Google 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. doi:10.1037/0012-1649.33.6.906Google Scholar
Shin, L. M., & Liberzon, I. (2010). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology, 35, 69–91. doi:10.1038/npp.2009.83Google Scholar
Silvers, J. A., Insel, C., Powers, A., Franz, P., Helion, C., Martin, R. E., … Ochsner, K. N. (2017). VlPFC-vmPFC-amygdala interactions underlie age-related differences in cognitive regulation of emotion. Cerebral Cortex, 27, 3502–3514. doi:10.1093/cercor/bhw073Google Scholar
Šimic, M. (2012). Zapažanja o jeziku akademijina brevijara (hazu III c 12). Slovo, 13, 245–266. doi:10.1038/nrn3313Google Scholar
Skowron, E. A., Cipriano-Essel, E., Gatzke-Kopp, L. M., Teti, D. M., & Ammerman, R. T. (2014). Early adversity, RSA, and inhibitory control: Evidence of children's neurobiological sensitivity to social context. Developmental Psychobiology, 56, 964–978. doi:10.1002/dev.21175Google Scholar
Slopen, N., Shonkoff, J. P., Albert, M. A., Yoshikawa, H., Jacobs, A., Stoltz, R., & Williams, D. R. (2016). Racial disparities in child adversity in the U.S.: Interactions with family immigration history and income. American Journal of Preventive Medicine, 50, 47–56. doi:10.1016/j.amepre.2015.06.013Google Scholar
Smith, A. M., Lewis, B. K., Ruttimann, U. E., Ye, F. Q., Sinnwell, T. M., Yang, Y., … Frank, J. A. (1999). Investigation of low frequency drift in fMRI signal. NeuroImage, 9, 526–533. doi:10.1006/nimg.1999.0435Google Scholar
Smith, R., Thayer, J. F., Khalsa, S. S., & Lane, R. D. (2017). The hierarchical basis of neurovisceral integration. Neuroscience and Biobehavioral Reviews, 75, 274–296. doi:10.1016/j.neubiorev.2017.02.003Google Scholar
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-Berg, H., … Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23, S208–S219. doi:10.1016/j.neuroimage.2004.07.051Google Scholar
Smokowski, P. R., & Bacallao, M. L. (2007). Acculturation, internalizing mental health symptoms, and self-esteem: Cultural experiences of Latino adolescents in North Carolina. Child Psychiatry and Human Development, 37, 273–292. doi:10.1007/s10578-006-0035-4Google Scholar
Suzuki, H., Luby, J. L., Botteron, K. N., Dietrich, R., McAvoy, M. P., & Barch, D. M. (2014). Early life stress and trauma and enhanced limbic activation to emotionally valenced faces in depressed and healthy children. Journal of the American Academy of Child & Adolescent Psychiatry, 53, 800–816. doi:10.1016/j.jaac.2014.04.013Google 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. doi:10.1176/appi.ajp.2014.14020195Google Scholar
Thayer, J. F., Åhs, F., Fredrikson, M., Sollers, J. J., & Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health. Neuroscience and Biobehavioral Reviews, 36, 747–756. doi:10.1016/j.neubiorev.2011.11.009Google Scholar
Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience and Biobehavioral Reviews, 33, 81–88. doi:10.1016/j.neubiorev.2008.08.004Google Scholar
Troop-Gordon, W. (2017). Peer victimization in adolescence: The nature, progression, and consequences of being bullied within a developmental context. Journal of Adolescence, 55, 116–128. doi:10.1016/j.adolescence.2016.12.012Google Scholar
Umaña-Taylor, A. J., & Updegraff, K. A. (2007). Latino adolescents’ mental health: Exploring the interrelations among discrimination, ethnic identity, cultural orientation, self-esteem, and depressive symptoms. Journal of Adolescence, 30, 549–567. doi:10.1016/j.adolescence.2006.08.002Google Scholar
Updegraff, K. A., McHale, S. M., Whiteman, S. D., Thayer, S. M., & Crouter, A. C. (2006). The nature and correlates of Mexican-American adolescents’ time with parents and peers. Child Development, 77, 1470–1486. doi:10.1111/j.1467-8624.2006.00948.xGoogle Scholar
VanTieghem, M. R., & Tottenham, N. (2016). Neurobiological programming of early life stress: Functional development of amygdala-prefrontal circuitry and vulnerability for stress-related psychopathology. In Brain imaging in behavioral neuroscience (pp. 289–320). Berlin: Springer.Google Scholar
Vilgis, V., Gelardi, K. L., Helm, J. L., Forbes, E. E., Hipwell, A. E., Keenan, K., & Guyer, A. E. (2018). Dorsomedial prefrontal activity to sadness predicts later emotion suppression and depression severity in adolescent girls. Child Development, 89, 758–772. doi:10.1111/cdev.13023Google Scholar
Watson, D., & Clark, L. A. (1991). The mood and anxiety symptom questionnaire. Unpublished manuscript, University of Iowa, Department of Psychology, Iowa City.Google Scholar
Weissman, D. G., Gelardi, K. L., Conger, R. D., Robins, R. W., Hastings, P. D., & Guyer, A. E. (2018). Adolescent externalizing problems: Contributions of community crime exposure and neural function during emotion introspection in Mexican-origin youth. Journal of Research on Adolescence, 28, 551–563. doi:10.1111/jora.12358Google Scholar
Weissman, D. G., Guyer, A. E., Ferrer, E., Robins, R. W., & Hastings, P. D. (2018). Adolescents’ brain-autonomic coupling during emotion processing. NeuroImage, 183, 818–827. doi:10.1016/j.neuroimage.2018.08.069Google Scholar
Wolf, R. C., & Herringa, R. J. (2016). Prefrontal-amygdala dysregulation to threat in pediatric posttraumatic stress disorder. Neuropsychopharmacology, 41, 822–831. doi:10.1038/npp.2015.209Google Scholar
Zhang, S., Hu, S., Chao, H. H., Ide, J. S., Luo, X., Farr, O. M., & Li, C. R. (2014). Ventromedial prefrontal cortex and the regulation of physiological arousal. Social Cognitive and Affective Neuroscience, 9, 900–908. doi:10.1093/scan/nst064Google Scholar
Zhang, S., Hu, S., Chao, H. H., Luo, X., Farr, O. M., & Li, C. R. (2012). Cerebral correlates of skin conductance responses in a cognitive task. NeuroImage, 62, 1489–1498. doi:10.1016/j.neuroimage.2012.05.036Google Scholar