Hostname: page-component-76d6cb85b7-5qg8f Total loading time: 0 Render date: 2026-07-15T17:22:52.646Z Has data issue: false hasContentIssue false
  • English
  • Français

Affective modulation of the startle response among children at high and low risk for anxiety disorders

Published online by Cambridge University Press:  27 April 2015

A. Kujawa ,
C. R. Glenn ,
G. Hajcak  and
D. N. Klein
A. Kujawa*
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY, USA
C. R. Glenn
Affiliation:
Department of Psychology, Harvard University, Cambridge, MA, USA
G. Hajcak
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY, USA
D. N. Klein
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, NY, USA
*
* Address for correspondence: Ms A. Kujawa, Department of Psychology, Stony Brook University, Stony Brook, NY 11794-2500, USA. (Email: autumn.kujawa@stonybrook.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Identifying early markers of risk for anxiety disorders in children may aid in understanding underlying mechanisms and informing prevention efforts. Affective modulation of the startle response indexes sensitivity to pleasant and unpleasant environmental contexts and has been shown to relate to anxiety, yet the extent to which abnormalities in affect-modulated startle reflect vulnerability for anxiety disorders in children has yet to be examined. The current study assessed the effects of parental psychopathology on affective modulation of startle in offspring.

Method

Nine-year-old children (n = 144) with no history of anxiety or depressive disorders completed a passive picture viewing task in which eye-blink startle responses were measured during the presentation of pleasant, neutral, and unpleasant images.

Results

Maternal anxiety was associated with distinct patterns of affective modulation of startle in offspring, such that children with maternal histories of anxiety showed potentiation of the startle response while viewing unpleasant images, but not attenuation during pleasant images, whereas children with no maternal history of anxiety exhibited attenuation of the startle response during pleasant images, but did not exhibit unpleasant potentiation – even when controlling for child symptoms of anxiety and depression. No effects of maternal depression or paternal psychopathology were observed.

Conclusions

These findings suggest that both enhanced startle responses in unpleasant conditions and failure to inhibit startle responses in pleasant conditions may reflect early emerging vulnerabilities that contribute to the later development of anxiety disorders.

Keywords

Anxietychildrenemotionriskstartle

Information

Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 12 , September 2015 , pp. 2647 - 2656
Copyright
Copyright © Cambridge University Press 2015 

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.)

Article purchase

Temporarily unavailable

References

Allen, NB, Trinder, J, Brennan, C (1999). Affective startle modulation in clinical depression: preliminary findings. Biological Psychiatry 46, 542–550.CrossRefGoogle ScholarPubMed
Andreasen, NC, Endicott, J, Spitzer, RL, Winokur, G (1977). The family history method using diagnostic criteria: reliability and validity. Archives of General Psychiatry 34, 1229–1235.CrossRefGoogle ScholarPubMed
Axelson, D, Birmaher, B, Zelazny, J, Kaufman, J, Gill, MK (2009). The Schedule for Affective Disorders and Schizophrenia – Present and Lifetime Version (K-SADS-PL) 2009 working draft. Advanced Centre for Intervention and Services Research, Western Psychiatric Institute and Clinics. (http://www.Psychiatry.Pitt.Edu/research/tools-research/ksads-pl-2009-working-draft).Google Scholar
Bakker, MJ, Tijssen, MAJ, Van Der Meer, JN, Koelman, JHTM, Boer, F (2009). Increased whole-body auditory startle reflex and autonomic reactivity in children with anxiety disorders. Journal of Psychiatry & Neuroscience 34, 314–322.Google ScholarPubMed
Barker, TV, Reeb-Sutherland, BC, Fox, NA (2014). Individual differences in fear potentiated startle in behaviorally inhibited children. Developmental Psychobiology 56, 133–141.CrossRefGoogle ScholarPubMed
Benjamini, Y, Hochberg, Y (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57, 289–300.Google Scholar
Birmaher, B, Khetarpal, S, Brent, D, Cully, M, Balach, L, Kaufman, J, Neer, SM (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.CrossRefGoogle ScholarPubMed
Blumenthal, TD, Cuthbert, BN, Filion, DL, Hackley, S, Lipp, OV, Van Boxtel, A (2005). Committee report: guidelines for human startle eyeblink electromyographic studies. Psychophysiology 42, 1–15.CrossRefGoogle ScholarPubMed
Bögels, S, Phares, V (2008). Fathers’ role in the etiology, prevention, and treatment of child anxiety: a review and new model. Clinical Psychology Review 28, 539–558.CrossRefGoogle ScholarPubMed
Bradley, MM, Cuthbert, BN, Lang, PJ (1990). Startle reflex modification: emotion or attention? Psychophysiology 27, 513–522.CrossRefGoogle ScholarPubMed
Bradley, MM, Cuthbert, BN, Lang, PJ (1993). Pictures as prepulse: attention and emotion in startle modification. Psychophysiology 30, 541–545.CrossRefGoogle ScholarPubMed
Britton, JC, Grillon, C, Lissek, S, Norcross, MA, Szuhany, KL, Chen, G, Ernst, M, Nelson, EE, Leibenluft, E, Schechner, T, Pine, DS (2013). Response to learned threat: an fMRI study in adolescent and adult anxiety. American Journal of Psychiatry 170, 1195–1204.CrossRefGoogle ScholarPubMed
Cornwell, BR, Johnson, L, Berardi, L, Grillon, C (2006). Anticipation of public speaking in virtual reality reveals a relationship between trait social anxiety and startle reactivity. Biological Psychiatry 59, 664–666.CrossRefGoogle ScholarPubMed
Craske, MG, Wolitzky-Taylor, KB, Mineka, S, Zinbarg, R, Waters, AM, Vrshek-Schallhorn, S, Epstein, A, Naliboff, B, Ornitz, E (2012). Elevated responding to safe conditions as a specific risk factor for anxiety versus depressive disorders: evidence from a longitudinal investigation. Journal of Abnormal Psychology 121, 315.CrossRefGoogle ScholarPubMed
De Jong, P, Merckelbach, H, Arntz, A (1991). Eyeblink startle responses in spider phobies before and after treatment: a pilot study. Journal of Psychopathology and Behavioral Assessment 13, 213–223.CrossRefGoogle Scholar
De Jong, P, Visser, S, Merckelbach, H (1996). Startle and spider phobia: unilateral probes and the prediction of treatment effects. Journal of Psychophysiology 10, 150–160.Google Scholar
Dichter, GS, Tomarken, AJ (2008). The chronometry of affective startle modulation in unipolar depression. Journal of Abnormal Psychology 117, 1–15.CrossRefGoogle ScholarPubMed
Dichter, GS, Tomarken, AJ, Shelton, RC, Sutton, SK (2004). Early- and late-onset startle modulation in unipolar depression. Psychophysiology 41, 433–440.CrossRefGoogle ScholarPubMed
Donovan, CL, Spence, SH (2000). Prevention of childhood anxiety disorders. Clinical Psychology Review 20, 509–531.CrossRefGoogle ScholarPubMed
Fava, M, Rankin, MA, Wright, EC, Alpert, JE, Nierenberg, AA, Pava, J, Rosenbaum, JF (2000). Anxiety disorders in major depression. Comprehensive Psychiatry 41, 97–102.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1996). The Structured Clinical Interview for DSM-IV Axis I Disorders - Non-Patient Editions. Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
Forbes, EE, Miller, A, Cohn, JF, Fox, NA, Kovacs, M (2005). Affect-modulated startle in adults with childhood-onset depression: relations to bipolar course and number of lifetime depressive episodes. Psychiatry Research 134, 11–25.CrossRefGoogle ScholarPubMed
Glenn, CR, Klein, DN, Lissek, S, Britton, JC, Pine, DS, Hajcak, G (2012). The development of fear learning and generalization in 8–13 year olds. Developmental Psychobiology 54, 675–684.CrossRefGoogle ScholarPubMed
Grillon, C (2002). Startle reactivity and anxiety disorders: aversive conditioning, context, and neurobiology. Biological Psychiatry 52, 958–975.CrossRefGoogle ScholarPubMed
Grillon, C, Baas, J (2003). A review of the modulation of the startle reflex by affective states and its application in psychiatry. Clinical Neurophysiology 114, 1557–1579.CrossRefGoogle ScholarPubMed
Grillon, C, Dierker, L, Merikangas, KR (1997). Startle modulation in children at risk for anxiety disorders and/or alcoholism. Journal of the American Academy of Child & Adolescent Psychiatry 36, 925–932.CrossRefGoogle ScholarPubMed
Grillon, C, Dierker, L, Merikangas, KR (1998). Fear-potentiated startle in adolescent offspring of parents with anxiety disorders. Biological Psychiatry 44, 990–997.CrossRefGoogle ScholarPubMed
Ingram, RE, Luxton, DD (2005). Vulnerability-stress models. In Development of Psychopathology: A Vulnerability-Stress Perspective (ed. Hankin, B. L. and Abela, J. R. Z.), pp. 32–46. Sage Publications: Thousand Oaks.CrossRefGoogle Scholar
Jovanovic, T, Nylocks, KM, Gamwell, KL, Smith, A, Davis, TA, Norrholm, SD, Bradley, B (2014). Development of fear acquisition and extinction in children: effects of age and anxiety. Neurobiology of Learning and Memory 113, 135–142.CrossRefGoogle ScholarPubMed
Kaviani, H, Gray, J, Checkley, S, Raven, P, Wilson, G, Kumari, V (2004). Affective modulation of the startle response in depression: influence of the severity of depression, anhedonia, and anxiety. Journal of Affective Disorders 83, 21–31.CrossRefGoogle ScholarPubMed
Kendler, KS, Neale, MC, Kessler, RC, Heath, AC, Eaves, LJ (1992). The genetic epidemiology of phobias in women: the interrelationship of agoraphobia, social phobia, situational phobia, and simple phobia. Archives of General Psychiatry 49, 273–281.CrossRefGoogle ScholarPubMed
Kessler, RC, Chiu, WT, Demler, O, Walters, EE (2005). Prevalence, severity, and comorbidity of 12-month dsm-iv disorders in the national comorbidity survey replication. Archives of General Psychiatry 62, 617–627.CrossRefGoogle ScholarPubMed
Kovacs, M (1992). Children's Depression Inventory. Multi-Health Systems: Toronto.Google Scholar
Kraemer, HC, Kazdin, AE, Offord, DR, Kessler, RC, Jensen, PS, Kupfer, DJ (1997). Coming to terms with the terms of risk. Archives of General Psychiatry 54, 337–343.CrossRefGoogle ScholarPubMed
Kujawa, A, Proudfit, GH, Klein, DN (2014). Neural reactivity to rewards and losses in offspring of mothers and fathers with histories of depressive and anxiety disorders. Journal of Abnormal Psychology 123, 287–297.CrossRefGoogle ScholarPubMed
Lang, PJ, Bradley, MM, Cuthbert, BN (1990). Emotion, attention, and the startle reflex. Psychological Review 97, 377–395.CrossRefGoogle ScholarPubMed
Lang, PJ, Bradley, MM, Cuthbert, BN (2008). International Affective Picture System (IAPS): Affective Ratings of Pictures and Instructional Manual. Technical report A-8. University of Florida: Gainesville.Google Scholar
Lang, PJ, McTeague, LM (2009). The anxiety disorder spectrum: fear imagery, physiological reactivity, and differential diagnosis. Anxiety, Stress & Coping 22, 5–25.CrossRefGoogle ScholarPubMed
Larson, CL, Nitschke, JB, Davidson, RJ (2007). Common and distinct patterns of affective response in dimensions of anxiety and depression. Emotion 7, 182–191.CrossRefGoogle ScholarPubMed
McClure, EB, Brennan, PA, Hammen, C, Le Brocque, RM (2001). Parental anxiety disorders, child anxiety disorders, and the perceived parent–child relationship in an Australian high-risk sample. Journal of Abnormal Child Psychology 29, 1–10.CrossRefGoogle Scholar
McTeague, LM, Lang, PJ (2012). The anxiety spectrum and the reflex physiology of defense: from circumscribed fear to broad distress. Depression and Anxiety 29, 264–281.CrossRefGoogle ScholarPubMed
McTeague, LM, Lang, PJ, Wangelin, BC, Laplante, MC, Bradley, MM (2012). Defensive mobilization in specific phobia: fear specificity, negative affectivity, and diagnostic prominence. Biological Psychiatry 72, 8–18.CrossRefGoogle ScholarPubMed
Melzig, CA, Weike, AI, Zimmermann, J, Hamm, AO (2007). Startle reflex modulation and autonomic responding during anxious apprehension in panic disorder patients. Psychophysiology 44, 846–854.CrossRefGoogle ScholarPubMed
Merikangas, KR, Avenevoli, S, Dierker, L, Grillon, C (1999). Vulnerability factors among children at risk for anxiety disorders. Biological Psychiatry 46, 1523–1535.CrossRefGoogle ScholarPubMed
Merikangas, KR, Dierker, LC, Szatmari, P (1998). Psychopathology among offspring of parents with substance abuse and/or anxiety disorders: a high-risk study. Journal of Child Psychology and Psychiatry 39, 711–720.Google ScholarPubMed
Nelson, BD, Mcgowan, SK, Sarapas, C, Robison-Andrew, EJ, Altman, SE, Campbell, ML, Gorka, SM, Katz, AC, Shankman, SA (2013). Biomarkers of threat and reward sensitivity demonstrate unique associations with risk for psychopathology. Journal of Abnormal Psychology 122, 662–671.CrossRefGoogle ScholarPubMed
Olino, TM, Klein, DN, Dyson, MW, Rose, SA, Durbin, CE (2010). Temperamental emotionality in preschool-aged children and depressive disorders in parents: associations in a large community sample. Journal of Abnormal Psychology 119, 468–478.CrossRefGoogle Scholar
Öst, L-G, Hugdahl, K (1981). Acquisition of phobias and anxiety response patterns in clinical patients. Behaviour Research and Therapy 19, 439–447.CrossRefGoogle ScholarPubMed
Reeb-Sutherland, BC, Helfinstein, SM, Degnan, KA, Pérez-Edgar, K, Henderson, HA, Lissek, S, Chronis-Tuscano, A, Grillon, C, Pine, DS, Fox, NA (2009). Startle response in behaviorally inhibited adolescents with a lifetime occurrence of anxiety disorders. Journal of the American Academy of Child & Adolescent Psychiatry 48, 610–617.CrossRefGoogle ScholarPubMed
Rohde, P, Lewinsohn, PM, Klein, DN, Seeley, JR (2005). Association of parental depression with psychiatric course from adolescence to young adulthood among formerly depressed individuals. Journal of Abnormal Psychology 114, 409–420.CrossRefGoogle ScholarPubMed
Shankman, SA, Nelson, BD, Sarapas, C, Robison-Andrew, EJ, Campbell, ML, Altman, SE, Mcgowan, SK, Katz, AC, Gorka, SM (2013). A psychophysiological investigation of threat and reward sensitivity in individuals with panic disorder and/or major depressive disorder. Journal of Abnormal Psychology 122, 322–328.CrossRefGoogle ScholarPubMed
Sobin, C, Weissman, MM, Goldstein, RB, Adams, P (1993). Diagnostic interviewing for family studies: comparing telephone and face-to-face methods for the diagnosis of lifetime psychiatric disorders. Psychiatric Genetics 3, 227–233.CrossRefGoogle Scholar
Taylor-Clift, A, Morris, B, Rottenberg, J, Kovacs, M (2011). Emotion-modulated startle in anxiety disorders is blunted by co-morbid depressive episodes. Psychological Medicine 41, 129–139.CrossRefGoogle ScholarPubMed
Vaidyanathan, U, Patrick, CJ, Cuthbert, BN (2009). Linking dimensional models of internalizing psychopathology to neurobiological systems: affect-modulated startle as an indicator of fear and distress disorders and affiliated traits. Psychological Bulletin 135, 909–942.CrossRefGoogle ScholarPubMed
Vrana, SR, Constantine, JA, Westman, JS (1992). Startle reflex modification as an outcome measure in the treatment of phobia: two case studies. Behavioral Assessment 14, 279–291.Google Scholar
Vrana, SR, Spence, EL, Lang, PJ (1988). The startle probe response: a new measure of emotion? Journal of Abnormal Psychology 97, 487–491.CrossRefGoogle ScholarPubMed
Waters, AM, Lipp, OV, Spence, SH (2005). The effects of affective picture stimuli on blink modulation in adults and children. Biological Psychology 68, 257–281.CrossRefGoogle ScholarPubMed
Waters, AM, Nazarian, M, Mineka, S, Zinbarg, RE, Griffith, JW, Naliboff, B, Ornitz, EM, Craske, MG (2014). Context and explicit threat cue modulation of the startle reflex: preliminary evidence of distinctions between adolescents with principal fear disorders versus distress disorders. Psychiatry Research 217, 93–99.CrossRefGoogle ScholarPubMed
Waters, AM, Neumann, DL, Henry, J, Craske, MG, Ornitz, EM (2008). Baseline and affective startle modulation by angry and neutral faces in 4–8-year-old anxious and non-anxious children. Biological Psychology 78, 10–19.CrossRefGoogle ScholarPubMed
Zvolensky, MJ, Schmidt, NB, Bernstein, A, Keough, ME (2006). Risk-factor research and prevention programs for anxiety disorders: a translational research framework. Behaviour Research and Therapy 44, 1219–1239.CrossRefGoogle ScholarPubMed