Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-25T16:07:12.215Z Has data issue: false hasContentIssue false
  • English
  • Français

Levels of early-childhood behavioral inhibition predict distinct neurodevelopmental pathways to pediatric anxiety

Published online by Cambridge University Press:  08 January 2019

Rany Abend ,
Caroline Swetlitz ,
Lauren K. White ,
Tomer Shechner ,
Yair Bar-Haim ,
Courtney Filippi ,
Katharina Kircanski ,
Simone P. Haller ,
Brenda E. Benson  and
Gang Chen
...Show all authors
Rany Abend*
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Caroline Swetlitz
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Lauren K. White
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA Childrenʼs Hospital of Philadelphia, Philadelphia, PA, USA
Tomer Shechner
Affiliation:
Psychology Department, University of Haifa, Haifa, Israel
Yair Bar-Haim
Affiliation:
School of Psychological Sciences and Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel
Courtney Filippi
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
Simone P. Haller
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Brenda E. Benson
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Gang Chen
Affiliation:
Scientific and Statistical Computing Core, National Institute of Mental Health, Bethesda, MD, USA
Ellen Leibenluft
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
Nathan A. Fox
Affiliation:
Department of Human Development and Quantitative Methodology, University of Maryland, College Park, MD, USA
Daniel S. Pine
Affiliation:
Emotion and Development Branch, National Institute of Mental Health, Bethesda, MD, USA
*
Author for correspondence: Rany Abend, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Anxiety symptoms gradually emerge during childhood and adolescence. Individual differences in behavioral inhibition (BI), an early-childhood temperament, may shape developmental paths through which these symptoms arise. Cross-sectional research suggests that level of early-childhood BI moderates associations between later anxiety symptoms and threat-related amygdala–prefrontal cortex (PFC) circuitry function. However, no study has characterized these associations longitudinally. Here, we tested whether level of early-childhood BI predicts distinct evolving associations between amygdala–PFC function and anxiety symptoms across development.

Methods

Eighty-seven children previously assessed for BI level in early childhood provided data at ages 10 and/or 13 years, consisting of assessments of anxiety and an fMRI-based dot-probe task (including threat, happy, and neutral stimuli). Using linear-mixed-effects models, we investigated longitudinal changes in associations between anxiety symptoms and threat-related amygdala–PFC connectivity, as a function of early-childhood BI.

Results

In children with a history of high early-childhood BI, anxiety symptoms became, with age, more negatively associated with right amygdala–left dorsolateral-PFC connectivity when attention was to be maintained on threat. In contrast, with age, low-BI children showed an increasingly positive anxiety–connectivity association during the same task condition. Behaviorally, at age 10, anxiety symptoms did not relate to fluctuations in attention bias (attention bias variability, ABV) in either group; by age 13, low-BI children showed a negative anxiety–ABV association, whereas high-BI children showed a positive anxiety–ABV association.

Conclusions

Early-childhood BI levels predict distinct neurodevelopmental pathways to pediatric anxiety symptoms. These pathways involve distinct relations among brain function, behavior, and anxiety symptoms, which may inform diagnosis and treatment.

Keywords

Amygdalaanxietyattentionbehavioral inhibitionchildrenconnectivitydevelopmentalfMRIprefrontal cortex
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 1 , January 2020 , pp. 96 - 106
Copyright
Copyright © Cambridge University Press 2019 

Access options

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

References

Abend, R, De Voogd, EL, Salemink, E, Wiers, RW, Perez-Edgar, K, Fitzgerald, A, White, LK, Salum, GA, He, J, Silverman, WK, Pettit, JW, Pine, DS and Bar-Haim, Y (2018) Association between attention bias to threat and anxiety symptoms in children and adolescents. Depression and Anxiety 35, 229–238.Google Scholar
Bar-Haim, Y, Lamy, D, Pergamin, L, Bakermans-Kranenburg, MJ and Van Ijzendoorn, MH (2007) Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychological Bulletin 133, 1–24.Google Scholar
Barker, TV, Reeb-Sutherland, B, Degnan, KA, Walker, OL, Chronis-Tuscano, A, Henderson, HA, Pine, DS and Fox, NA (2015) Contextual startle responses moderate the relation between behavioral inhibition and anxiety in middle childhood. Psychophysiology 52, 1544–1549.Google Scholar
Beesdo, K, Knappe, S and Pine, DS (2009) Anxiety and anxiety disorders in children and adolescents: developmental issues and implications for DSM-V. Psychiatric Clinics of North America 32, 483–524.Google Scholar
Birmaher, B, Khetarpal, S, Brent, D, Cully, M, Balach, L, Kaufman, J and Neer, SM (1997) The screen for child anxiety related emotional disorders (SCARED): scale construction and psychometric characteristics. Journal of the American Academy of Child and Adolescent Psychiatry 36, 545–553.Google Scholar
Birmaher, B, Brent, DA, Chiappetta, L, Bridge, J, Monga, S and Baugher, M (1999) Psychometric properties of the Screen for Child Anxiety Related Emotional Disorders (SCARED): a replication study. Journal of the American Academy of Child and Adolescent Psychiatry 38, 1230–1236.Google Scholar
Birn, RM, Shackman, AJ, Oler, JA, Williams, LE, Mcfarlin, DR, Rogers, GM, Shelton, SE, Alexander, AL, Pine, DS, Slattery, MJ, Davidson, RJ, Fox, AS and Kalin, NH (2014) Evolutionarily conserved prefrontal-amygdalar dysfunction in early-life anxiety. Molecular Psychiatry 19, 915–922.Google Scholar
Bishop, SJ (2007) Neurocognitive mechanisms of anxiety: an integrative account. Trends in Cognitive Sciences 11, 307–316.Google Scholar
Bishop, SJ (2008) Neural mechanisms underlying selective attention to threat. Annals of the New York Academy of Sciences 1129, 141–152.Google Scholar
Britton, JC, Bar-Haim, Y, Carver, FW, Holroyd, T, Norcross, MA, Detloff, A, Leibenluft, E, Ernst, M and Pine, DS (2012) Isolating neural components of threat bias in pediatric anxiety. Journal of Child Psychology and Psychiatry 53, 678–686.Google Scholar
Buzzell, GA, Troller-Renfree, SV, Barker, TV, Bowman, LC, Chronis-Tuscano, A, Henderson, HA, Kagan, J, Pine, DS and Fox, NA (2017) A neurobehavioral mechanism linking behaviorally inhibited temperament and later adolescent social anxiety. Journal of the American Academy of Child and Adolescent Psychiatry 56, 1097–1105.Google Scholar
Casey, BJ, Glatt, CE and Lee, FS (2015) Treating the developing versus developed brain: translating preclinical mouse and human studies. Neuron 86, 1358–1368.Google Scholar
Caspi, A, Moffitt, TE, Newman, DL and Silva, PA (1996) Behavioral observations at age 3 years predict adult psychiatric disorders – longitudinal evidence from a birth cohort. Archives of General Psychiatry 53, 1033–1039.Google Scholar
Chen, G, Saad, ZS, Britton, JC, Pine, DS and Cox, RW (2013) Linear mixed-effects modeling approach to FMRI group analysis. Neuroimage 73, 176–190.Google Scholar
Chronis-Tuscano, A, Degnan, KA, Pine, DS, Perez-Edgar, K, Henderson, HA, Diaz, Y, Raggi, VL and Fox, NA (2009) Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. Journal of the American Academy of Child and Adolescent Psychiatry 48, 928–935.Google Scholar
Cisler, JM and Koster, EH (2010) Mechanisms of attentional biases towards threat in anxiety disorders: an integrative review. Clinical Psychology Review 30, 203–216.Google Scholar
Cole, CE, Zapp, DJ, Fettig, NB and Perez-Edgar, K (2016) Impact of attention biases to threat and effortful control on individual variations in negative affect and social withdrawal in very young children. Journal of Experimental Child Psychology 141, 210–221.Google Scholar
Cox, RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research 29, 162–173.Google Scholar
Cox, RW, Chen, G, Glen, DR, Reynolds, RC and Taylor, PA (2017) FMRI clustering in AFNI: false-positive rates redux. Brain Connectivity 7, 152–171.Google Scholar
Cuthbert, BN (2015) Research domain criteria: toward future psychiatric nosologies. Dialogues in Clinical Neuroscience 17, 89–97.Google Scholar
Donders, AR, Van Der Heijden, GJ, Stijnen, T and Moons, KG (2006) Review: a gentle introduction to imputation of missing values. Journal of Clinical Epidemiology 59, 1087–1091.Google Scholar
Eklund, A, Nichols, TE and Knutsson, H (2016) Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the United States of America 113, 7900–7905.Google Scholar
Etkin, A, Buchel, C and Gross, JJ (2015) The neural bases of emotion regulation. Nature Reviews Neuroscience 16, 693–700.Google Scholar
Filkowski, MM and Haas, BW (2017) Rethinking the use of neutral faces as a baseline in fMRI neuroimaging studies of axis-I psychiatric disorders. Journal of Neuroimaging 27, 281–291.Google Scholar
Fox, AS and Kalin, NH (2014) A translational neuroscience approach to understanding the development of social anxiety disorder and its pathophysiology. American Journal of Psychiatry 171, 1162–1173.Google Scholar
Fox, NA and Pine, DS (2012) Temperament and the emergence of anxiety disorders. Journal of the American Academy of Child and Adolescent Psychiatry 51, 125–128.Google Scholar
Fox, NA, Schmidt, LA and Henderson, HA (2000) Developmental psychophysiology: conceptual and methodological perspectives. In T, CJ, Tassinary, LG and Berntson, GG (eds), Handbook of Psychophysiology, 2nd Edn. Cambridge: Cambridge University Press.Google Scholar
Fox, NA, Henderson, HA, Rubin, KH, Calkins, SD and Schmidt, LA (2001) Continuity and discontinuity of behavioral inhibition and exuberance: psychophysiological and behavioral influences across the first four years of life. Child Development 72, 1–21.Google Scholar
Fox, NA, Henderson, HA, Marshall, PJ, Nichols, KE and Ghera, MM (2005) Behavioral inhibition: linking biology and behavior within a developmental framework. Annual Review of Psychology 56, 235–262.Google Scholar
Frenkel, TI, Fox, NA, Pine, DS, Walker, OL, Degnan, KA and Chronis-Tuscano, A (2015) Early childhood behavioral inhibition, adult psychopathology and the buffering effects of adolescent social networks: a twenty-year prospective study. Journal of Child Psychology and Psychiatry 56, 1065–1073.Google Scholar
Fu, X, Taber-Thomas, BC and Perez-Edgar, K (2017) Frontolimbic functioning during threat-related attention: relations to early behavioral inhibition and anxiety in children. Biological Psychology 122, 98–109.Google Scholar
Gee, DG, Humphreys, KL, Flannery, J, Goff, B, Telzer, EH, Shapiro, M, Hare, TA, Bookheimer, SY and Tottenham, N (2013) A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. Journal of Neuroscience 33, 4584–4593.Google Scholar
Gogtay, N, Giedd, JN, Lusk, L, Hayashi, KM, Greenstein, D, Vaituzis, AC, Nugent, TF III, Herman, DH, Clasen, LS, Toga, AW, Rapoport, JL and Thompson, PM (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the USA 101, 8174–8179.Google Scholar
Grupe, DW and Nitschke, JB (2013) Uncertainty and anticipation in anxiety: an integrated neurobiological and psychological perspective. Nature Reviews Neuroscience 14, 488–501.Google Scholar
Guyer, AE, Lau, JY, Mcclure-Tone, EB, Parrish, J, Shiffrin, ND, Reynolds, RC, Chen, G, Blair, RJ, Leibenluft, E, Fox, NA, Ernst, M, Pine, DS and Nelson, EE (2008) Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Archives of General Psychiatry 65, 1303–1312.Google Scholar
Hane, AA, Fox, NA, Henderson, HA and Marshall, PJ (2008) Behavioral reactivity and approach-withdrawal bias in infancy. Developmental Psychology 44, 1491–1496.Google Scholar
Hardee, JE, Benson, BE, Bar-Haim, Y, Mogg, K, Bradley, BP, Chen, G, Britton, JC, Ernst, M, Fox, NA, Pine, DS and Perez-Edgar, K (2013) Patterns of neural connectivity during an attention bias task moderate associations between early childhood temperament and internalizing symptoms in young adulthood. Biological Psychiatry 74, 273–279.Google Scholar
Iacoviello, BM, Wu, G, Abend, R, Murrough, JW, Feder, A, Fruchter, E, Levinstein, Y, Wald, I, Bailey, CR, Pine, DS, Neumeister, A, Bar-Haim, Y and Charney, DS (2014) Attention bias variability and symptoms of posttraumatic stress disorder. Journal of Traumatic Stress 27, 232–239.Google Scholar
Insel, T, Cuthbert, B, Garvey, M, Heinssen, R, Pine, DS, Quinn, K, Sanislow, C and Wang, P (2010) Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. American Journal of Psychiatry 167, 748–751.Google Scholar
Kessler, RC, Berglund, P, Demler, O, Jin, R, Merikangas, KR and Walters, EE (2005 a) Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication. Archives of General Psychiatry 62, 593–602.Google Scholar
Kessler, RC, Chiu, WT, Demler, O, Merikangas, KR and Walters, EE (2005 b) Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the national comorbidity survey replication. Archives of General Psychiatry 62, 617–627.Google Scholar
Kim, MJ, Loucks, RA, Palmer, AL, Brown, AC, Solomon, KM, Marchante, AN and Whalen, PJ (2011) The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behavioural Brain Research 223, 403–410.Google Scholar
Lahat, A, Lamm, C, Chronis-Tuscano, A, Pine, DS, Henderson, HA and Fox, NA (2014) Early behavioral inhibition and increased error monitoring predict later social phobia symptoms in childhood. Journal of the American Academy of Child & Adolescent Psychiatry 53, 447–455.Google Scholar
Lahat, A, Benson, BE, Pine, DS, Fox, NA and Ernst, M (2018) Neural responses to reward in childhood: relations to early behavioral inhibition and social anxiety. Social Cognitive and Affective Neuroscience 13, 281–289.Google Scholar
Lamm, C, Walker, OL, Degnan, KA, Henderson, HA, Pine, DS, Mcdermott, JM and Fox, NA (2014) Cognitive control moderates early childhood temperament in predicting social behavior in 7-year-old children: an ERP study. Developmental Science 17, 667–681.Google Scholar
Ledoux, JE (1996) The Emotional Brain: The Mysterious Underpinnings of Emotional Life. New York: Simon & Schuster.Google Scholar
Ledoux, JE and Pine, DS (2016) Using neuroscience to help understand fear and anxiety: a two-system framework. American Journal of Psychiatry 173, 1083–1093.Google Scholar
Lewis-Morrarty, E, Degnan, KA, Chronis-Tuscano, A, Rubin, KH, Cheah, CSL, Pine, DS, Henderon, HA and Fox, NA (2012) Maternal over-control moderates the association between early childhood behavioral inhibition and adolescent social anxiety symptoms. Journal of Abnormal Child Psychology 40, 1363–1373.Google Scholar
Macleod, C, Mathews, A and Tata, P (1986) Attentional bias in emotional disorders. Journal of Abnormal Psychology 95, 15–20.Google Scholar
Matta, TH, Flournoy, JC and Byrne, ML (2017) Making an unknown unknown a known unknown: missing data in longitudinal neuroimaging studies. Developmental Cognitive Neuroscience 33, 83–98.Google Scholar
Mcdermott, JM, Perez-Edgar, K, Henderson, HA, Chronis-Tuscano, A, Pine, DS and Fox, NA (2009) A history of childhood behavioral inhibition and enhanced response monitoring in adolescence are linked to clinical anxiety. Biological Psychiatry 65, 445–448.Google Scholar
Mclaren, DG, Ries, ML, Xu, G and Johnson, SC (2012) A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage 61, 1277–1286.Google Scholar
Michalska, KJ, Machlin, L, Moroney, E, Lowet, DS, Hettema, JM, Roberson-Nay, R, Averbeck, BB, Brotman, MA, Nelson, EE, Leibenluft, E and Pine, DS (2017) Anxiety symptoms and children's eye gaze during fear learning. Journal of Child Psychology and Psychiatry 58, 1276–1286.Google Scholar
Monk, CS, Mcclure, EB, Nelson, EE, Zarahn, E, Bilder, RM, Leibenluft, E, Charney, DS, Ernst, M and Pine, DS (2003) Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20, 420–428.Google Scholar
Monk, CS, Telzer, EH, Mogg, K, Bradley, BP, Mai, XQ, Louro, HMC, Chen, G, Mcclure-Tone, EB, Ernst, M and Pine, DS (2008) Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. Archives of General Psychiatry 65, 568–576.Google Scholar
Morales, S, Taber-Thomas, BC and Pérez-Edgar, KE (2017). Patterns of attention to threat across tasks in behaviorally inhibited children at risk for anxiety. Developmental Science 20, e12391.Google Scholar
Naim, R, Abend, R, Wald, I, Eldar, S, Levi, O, Fruchter, E, Ginat, K, Halpern, P, Sipos, ML, Adler, AB, Bliese, PD, Quartana, PJ, Pine, DS and Bar-Haim, Y (2015) Threat-Related attention bias variability and posttraumatic stress. American Journal of Psychiatry 172, 1242–1250.Google Scholar
Nicholson, AA, Rabellino, D, Densmore, M, Frewen, PA, Paret, C, Kluetsch, R, Schmahl, C, Theberge, J, Neufeld, RW, Mckinnon, MC, Reiss, J, Jetly, R and Lanius, RA (2017) The neurobiology of emotion regulation in posttraumatic stress disorder: amygdala downregulation via real-time fMRI neurofeedback. Human Brain Mapping 38, 541–560.Google Scholar
Paret, C, Ruf, M, Gerchen, MF, Kluetsch, R, Demirakca, T, Jungkunz, M, Bertsch, K, Schmahl, C and Ende, G (2016) fMRI neurofeedback of amygdala response to aversive stimuli enhances prefrontal-limbic brain connectivity. Neuroimage 125, 182–188.Google Scholar
Perez-Edgar, K, Bar-Haim, Y, Mcdermott, JM, Chronis-Tuscano, A, Pine, DS and Fox, NA (2010) Attention biases to threat and behavioral inhibition in early childhood shape adolescent social withdrawal. Emotion 10, 349–357.Google Scholar
Perez-Edgar, K, Reeb-Sutherland, BC, Mcdermott, JM, White, LK, Henderson, HA, Degnan, KA, Hane, AA, Pine, DS and Fox, NA (2011) Attention biases to threat link behavioral inhibition to social withdrawal over time in very young children. Journal of Abnormal Child Psychology 39, 885–895.Google Scholar
Perez-Edgar, K, Taber-Thomas, B, Auday, E and Morales, S (2014) Temperament and attention as core mechanisms in the early emergence of anxiety. Children and Emotion: New Insights into Developmental Affective Science 26, 42–56.Google Scholar
Perlman, SB and Pelphrey, KA (2011) Developing connections for affective regulation: age-related changes in emotional brain connectivity. Journal of Experimental Child Psychology 108, 607–620.Google Scholar
Pine, DS and Fox, NA (2015) Childhood antecedents and risk for adult mental disorders. Annual Review of Psychology 66, 459–485.Google Scholar
Pinheiro, JC and Bates, DM (2000) Mixed-effects Models in S and S-PLUS. New York: Springer.Google Scholar
Price, RB, Kuckertz, JM, Siegle, GJ, Ladouceur, CD, Silk, JS, Ryan, ND, Dahl, RE and Amir, N (2015) Empirical recommendations for improving the stability of the dot-probe task in clinical research. Psychological Assessment 27, 365–376.Google Scholar
Price, RB, Allen, KB, Silk, JS, Ladouceur, CD, Ryan, ND, Dahl, RE, Forbes, EE and Siegle, GJ (2016) Vigilance in the laboratory predicts avoidance in the real world: a dimensional analysis of neural, behavioral, and ecological momentary data in anxious youth. Developmental Cognitive Neuroscience 19, 128–136.Google Scholar
Prior, M, Smart, D, Sanson, A and Oberklaid, F (2000) Does shy-inhibited temperament in childhood lead to anxiety problems in adolescence? Journal of the American Academy of Child and Adolescent Psychiatry 39, 461–468.Google Scholar
Shanmugan, S, Wolf, DH, Calkins, ME, Moore, TM, Ruparel, K, Hopson, RD, Vandekar, SN, Roalf, DR, Elliott, MA, Jackson, C, Gennatas, ED, Leibenluft, E, Pine, DS, Shinohara, RT, Hakonarson, H, Gur, RC, Gur, RE and Satterthwaite, TD (2016) Common and dissociable mechanisms of executive system dysfunction across psychiatric disorders in youth. American Journal of Psychiatry 173, 517–526.Google Scholar
Shechner, T and Bar-Haim, Y (2016) Threat monitoring and attention-bias modification in anxiety and stress-related disorders. Current Directions in Psychological Science 25, 431–437.Google Scholar
Shechner, T, Britton, JC, Perez-Edgar, K, Bar-Haim, Y, Ernst, M, Fox, NA, Leibenluft, E and Pine, DS (2012) Attention biases, anxiety, and development: toward or away from threats or rewards? Depression and Anxiety 29, 282–294.Google Scholar
Shechner, T, Jarcho, JM, Wong, S, Leibenluft, E, Pine, DS and Nelson, EE (2017) Threats, rewards, and attention deployment in anxious youth and adults: an eye tracking study. Biological Psychology 122, 121–129.Google Scholar
Stoddard, J, Tseng, WL, Kim, P, Chen, G, Yi, J, Donahue, L, Brotman, MA, Towbin, KE, Pine, DS and Leibenluft, E (2017) Association of irritability and anxiety with the neural mechanisms of implicit face emotion processing in youths with psychopathology. JAMA Psychiatry 74, 95–103.Google Scholar
Thai, N, Taber-Thomas, BC and Perez-Edgar, KE (2016) Neural correlates of attention biases, behavioral inhibition, and social anxiety in children: an ERP study. Developmental Cognitive Neuroscience 19, 200–210.Google Scholar
Thomas, KM, Drevets, WC, Whalen, PJ, Eccard, CH, Dahl, RE, Ryan, ND and Casey, BJ (2001) Amygdala response to facial expressions in children and adults. Biological Psychiatry 49, 309–316.Google Scholar
Ulfig, N, Setzer, M and Bohl, J (2003) Ontogeny of the human amygdala. Annals of the New York Academy of Sciences 985, 22–33.Google Scholar
Van Bockstaele, B, Verschuere, B, Tibboel, H, De Houwer, J, Crombez, G and Koster, EH (2014) A review of current evidence for the causal impact of attentional bias on fear and anxiety. Psychological Bulletin 140, 682–721.Google Scholar
White, LK, Mcdermott, JM, Degnan, KA, Henderson, HA and Fox, NA (2011) Behavioral inhibition and anxiety: the moderating roles of inhibitory control and attention shifting. Journal of Abnormal Child Psychology 39, 735–747.Google Scholar
White, LK, Britton, JC, Sequeira, S, Ronkin, EG, Chen, G, Bar-Haim, Y, Shechner, T, Ernst, M, Fox, NA, Leibenluft, E and Pine, DS (2016) Behavioral and neural stability of attention bias to threat in healthy adolescents. Neuroimage 136, 84–93.Google Scholar
White, LK, Degnan, KA, Henderson, HA, Perez-Edgar, K, Walker, OL, Shechner, T, Leibenluft, E, Bar-Haim, Y, Pine, DS and Fox, NA (2017 a) Developmental relations among behavioral inhibition, anxiety, and attention biases to threat and positive information. Child Development 88, 141–155.Google Scholar
White, LK, Sequeira, S, Britton, JC, Brotman, MA, Gold, AL, Berman, E, Towbin, K, Abend, R, Fox, NA, Bar-Haim, Y, Leibenluft, E and Pine, DS (2017 b) Complementary features of attention bias modification therapy and cognitive-behavioral therapy in pediatric anxiety disorders. American Journal of Psychiatry 174, 775–784.Google Scholar
Wu, MJ, Kujawa, A, Lu, LH, Fitzgerald, DA, Klumpp, H, Fitzgerald, KD, Monk, CS and Phan, KL (2016) Age-related changes in amygdala-frontal connectivity during emotional face processing from childhood into young adulthood. Human Brain Mapping 37, 1684–1695.Google Scholar
Zvielli, A, Bernstein, A and Koster, EH (2015) Temporal dynamics of attentional bias. Clinical Psychological Science 3, 772–788.Google Scholar
Supplementary material: File

Abend et al. supplementary material

Abend et al. supplementary material 1

Download Abend et al. supplementary material(File)
File 58.5 KB
Supplementary material: Image

Abend et al. supplementary material

Abend et al. supplementary material 2

Download Abend et al. supplementary material(Image)
Image 33.3 KB
Supplementary material: Image

Abend et al. supplementary material

Abend et al. supplementary material 3

Download Abend et al. supplementary material(Image)
Image 44.1 KB
Supplementary material: Image

Abend et al. supplementary material

Abend et al. supplementary material 4

Download Abend et al. supplementary material(Image)
Image 279.1 KB