Hostname: page-component-848d4c4894-hfldf Total loading time: 0 Render date: 2024-06-12T20:24:24.171Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurobiological sensitivity to unpredictable threat and familial risk for the internalizing and externalizing spectra in adolescents

Published online by Cambridge University Press:  19 August 2022

Clare C. Beatty Open the ORCID record for Clare C. Beatty [Opens in a new window] ,
Rachel A. Ferry ,
Nicholas R. Eaton ,
Daniel N. Klein  and
Brady D. Nelson
Clare C. Beatty*
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, New York, USA
Rachel A. Ferry
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, New York, USA
Nicholas R. Eaton
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, New York, USA
Daniel N. Klein
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, New York, USA
Brady D. Nelson
Affiliation:
Department of Psychology, Stony Brook University, Stony Brook, New York, USA
*
Author for correspondence: Clare C. Beatty, E-mail: clare.beatty@stonybrook.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Adolescence is a key developmental period for the emergence of psychiatric disorders. However, there is still no consensus on the core mechanisms of dysfunction in youth. Neurobiological sensitivity to unpredictable threat has been associated with several psychiatric disorders in adults. The present study examined adolescent defensive motivation (startle reflex) and attention (event-related potentials) in anticipation of unpredictable threat in relation to both adolescent and maternal (i.e. familial risk) internalizing and externalizing spectra.

Methods

The sample included 395 15-year-old adolescents and their biological mothers. Adolescent startle potentiation and probe P300 suppression (indicating increased attention to threat) were measured in anticipation of predictable and unpredictable threat. Adolescent and maternal lifetime history of psychiatric disorders were assessed via semi-structured diagnostic interviews, and confirmatory factor analysis was used to model internalizing and externalizing spectra.

Results

The adolescent internalizing spectrum was positively associated with adolescent startle potentiation and probe P300 suppression to unpredictable threat. Conversely, the adolescent externalizing spectrum was negatively associated with adolescent P300 suppression to unpredictable threat. The maternal internalizing spectrum was positively associated with adolescent startle potentiation to unpredictable threat and P300 suppression to both predictable and unpredictable threat. The maternal externalizing spectrum was negatively associated with adolescent startle potentiation to unpredictable threat and P300 suppression to both predictable and unpredictable threat. Adolescent and maternal internalizing and externalizing spectra were independently related to adolescent startle potentiation and P300 suppression.

Conclusions

Adolescent neurobiological sensitivity to unpredictable threat is associated with both personal history and familial risk for the internalizing and externalizing spectra.

Keywords

AdolescenceERPsexternalizinginternalizingriskstartleunpredictability
Type
Original Article
Information
Psychological Medicine , Volume 53 , Issue 12 , September 2023 , pp. 5395 - 5404
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Bar-Haim, Y., Lamy, D., Pergamin, L., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin 133(1), 1–24. https://doi.org/10.1037/0033-2909.133.1.1.CrossRefGoogle ScholarPubMed
Bentler, P. M. (2006). EQS structural equations program manual. Retrieved 19 June 2022, from https://www.mvsoft.com/wp-content/uploads/2021/04/EQS_6_Prog_Manual_422pp.pdf.Google Scholar
Carleton, R. N. (2016). Into the unknown: A review and synthesis of contemporary models involving uncertainty. Journal of Anxiety Disorders, 39, 30–43. https://doi.org/10.1016/j.janxdis.2016.02.007.CrossRefGoogle ScholarPubMed
Cepeda, N. J., Cepeda, M. L., & Kramer, A. F. (2000). Task switching and attention deficit hyperactivity disorder. Journal of Abnormal Child Psychology, 28(3), 213–226. https://doi.org/10.1023/a:1005143419092.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Rogosch, F. A. (1996). Equifinality and multifinality in developmental psychopathology. Development and Psychopathology, 8(4), 597–600. https://doi.org/10.1017/S0954579400007318.CrossRefGoogle Scholar
Clark, C. R., McFarlane, A. C., Weber, D. L., & Battersby, M. (1996). Enlarged frontal P300 to stimulus change in panic disorder. Biological Psychiatry, 39(10), 845–856. https://doi.org/10.1016/0006-3223(95)00288-x.CrossRefGoogle ScholarPubMed
Conzelmann, A., Woidich, E., Mucha, R. F., Weyers, P., Jacob, C. P., Lesch, K.-P., & Pauli, P. (2011). Methylphenidate normalizes emotional processing in adult patients with attention-deficit/hyperactivity disorder: Preliminary findings. Brain Research, 1381, 159–166. https://doi.org/10.1016/j.brainres.2010.12.085.CrossRefGoogle ScholarPubMed
Copeland, W. E., Wolke, D., Shanahan, L., & Jane Costello, E. (2015). Adult functional outcomes of common childhood psychiatric problems. JAMA Psychiatry, 72(9), 892–899. https://doi.org/10.1001/jamapsychiatry.2015.0730.CrossRefGoogle ScholarPubMed
Correa, K. A., Li, L. Y., Nelson, B. D., & Shankman, S. A. (2022). Event-related potentials to acoustic startle probes during unpredictable threat are associated with individual differences in intolerance of uncertainty. International Journal of Psychophysiology, 174, 66–75. https://doi.org/10.1016/j.ijpsycho.2022.01.016.CrossRefGoogle ScholarPubMed
Crone, E. A., & Dahl, R. E. (2012). Understanding adolescence as a period of social-affective engagement and goal flexibility. Nature Reviews. Neuroscience, 13(9), 636–650. https://doi.org/10.1038/nrn3313.CrossRefGoogle ScholarPubMed
Diner, B. C., Holcomb, P. J., & Dykman, R. A. (1985). P300 in major depressive disorder. Psychiatry Research, 15(3), 175–184. https://doi.org/10.1016/0165-1781(85)90074-5.CrossRefGoogle ScholarPubMed
Enoch, M. A., White, K. V., Harris, C. R., Rohrbaugh, J. W., & Goldman, D. (2001). Alcohol use disorders and anxiety disorders: Relation to the P300 event-related potential. Alcoholism, Clinical and Experimental Research, 25(9), 1293–1300.CrossRefGoogle Scholar
Ferry, R. A., Beatty, C. C., Klein, D. N., & Nelson, B. D. (under review). Family study of the startle reflex and event related potentials in anticipation of predictable and unpredictable threat in adolescents and their parents.Google Scholar
Ferry, R. A., & Nelson, B. D. (2020). Differential impact of threat type on defensive motivation and attention during the NPU-threat task. Motivation and Emotion, 44(5), 670–685. https://doi.org/10.1007/s11031-020-09835-5.CrossRefGoogle Scholar
First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. W. (2007). The structured clinical interview for DSM-IV axis I disorders – non-patient edition. New York, NY: Biometrics Research Department, New York State Psychiatric Institute.Google Scholar
Gorka, S. M., Lieberman, L., Shankman, S. A., & Phan, K. L. (2017). Startle potentiation to uncertain threat as a psychophysiological indicator of fear-based psychopathology: An examination across multiple internalizing disorders. Journal of Abnormal Psychology, 126(1), 8–18. https://doi.org/10.1037/abn0000233.CrossRefGoogle ScholarPubMed
Gorka, S. M., & Shankman, S. A. (2017). Preliminary evidence that reactivity to uncertain threat is an endophenotype for alcohol use disorder. Drug and Alcohol Dependence, 180, 265–271. https://doi.org/10.1016/j.drugalcdep.2017.08.023.CrossRefGoogle ScholarPubMed
Gratton, G., Coles, M. G., & Donchin, E. (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology, 55(4), 468–484. https://doi.org/10.1016/0013-4694(83)90135-9.CrossRefGoogle ScholarPubMed
Grillon, C., Baas, J. P., Lissek, S., Smith, K., & Milstein, J. (2004). Anxious responses to predictable and unpredictable aversive events. Behavioral Neuroscience, 118(5), 916–924. https://doi.org/10.1037/0735-7044.118.5.916.CrossRefGoogle ScholarPubMed
Grillon, C., Dierker, L., & Merikangas, K. R. (1997). Startle modulation in children at risk for anxiety disorders and/or alcoholism. Journal of the American Academy of Child and Adolescent Psychiatry, 36(7), 925–932. https://doi.org/10.1097/00004583-199707000-00014.CrossRefGoogle ScholarPubMed
Grillon, C., Dierker, L., & Merikangas, K. R. (1998). Fear-potentiated startle in adolescent offspring of parents with anxiety disorders. Biological Psychiatry, 44(10), 990–997. https://doi.org/10.1016/s0006-3223(98)00188-7.CrossRefGoogle ScholarPubMed
Grillon, C., Lissek, S., Rabin, S., McDowell, D., Dvir, S., & Pine, D. S. (2008). Increased anxiety during anticipation of unpredictable but not predictable aversive stimuli as a psychophysiologic marker of panic disorder. The American Journal of Psychiatry, 165(7), 898–904. https://doi.org/10.1176/appi.ajp.2007.07101581.CrossRefGoogle Scholar
Grillon, C., Warner, V., Hille, J., Merikangas, K. R., Bruder, G. E., Tenke, C. E., … Weissman, M. M. (2005). Families at high and low risk for depression: A three-generation startle study. Biological Psychiatry, 57(9), 953–960. https://doi.org/10.1016/j.biopsych.2005.01.045.CrossRefGoogle ScholarPubMed
Grupe, D. W., & Nitschke, J. B. (2013). Uncertainty and anticipation in anxiety: An integrated neurobiological and psychological perspective. Nature Reviews. Neuroscience, 14(7), 488–501. https://doi.org/10.1038/nrn3524.CrossRefGoogle ScholarPubMed
Heitmann, J., Jonker, N. C., Ostafin, B. D., & de Jong, P. J. (2020). Attentional bias for alcohol cues in visual search-increased engagement, difficulty to disengage or both? PLoS One, 15(1), e0228272. https://doi.org/10.1371/journal.pone.0228272.CrossRefGoogle ScholarPubMed
Hu, L., & Bentler, P. M. (1999). Cutoff criteria for fit indexes in covariance structure analysis: Conventional criteria versus new alternatives. Structural Equation Modeling: A Multidisciplinary Journal, 6(1), 1–55. https://doi.org/10.1080/10705519909540118.CrossRefGoogle Scholar
Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., … Wang, P. (2010). Research domain criteria (RDoC): Toward a new classification framework for research on mental disorders. The American Journal of Psychiatry, 167(7), 748–751. https://doi.org/10.1176/appi.ajp.2010.09091379.CrossRefGoogle Scholar
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., … Ryan, N. (1997). Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry, 36(7), 980–988. https://doi.org/10.1097/00004583-199707000-00021.CrossRefGoogle ScholarPubMed
Kendler, K. S., Walters, E. E., Neale, M. C., Kessler, R. C., Heath, A. C., & Eaves, L. J. (1995). The structure of the genetic and environmental risk factors for six major psychiatric disorders in women: Phobia, generalized anxiety disorder, panic disorder, bulimia, major depression, and alcoholism. Archives of General Psychiatry, 52(5), 374–383.CrossRefGoogle ScholarPubMed
Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication. Archives of General Psychiatry, 62(6), 593–602. https://doi.org/10.1001/archpsyc.62.6.593.CrossRefGoogle ScholarPubMed
Klein, D. N., & Finsaas, M. C. (2017). The stony brook temperament study: Early antecedents and pathways to emotional disorders. Child Development Perspectives, 11(4), 257–263. https://doi.org/10.1111/cdep.12242.CrossRefGoogle Scholar
Kotov, R., Krueger, R. F., Watson, D., Achenbach, T. M., Althoff, R. R., Bagby, R. M., … Zimmerman, M. (2017). The hierarchical taxonomy of psychopathology (HiTOP): A dimensional alternative to traditional nosologies. Journal of Abnormal Psychology, 126(4), 454–477. https://doi.org/10.1037/abn0000258.CrossRefGoogle ScholarPubMed
Krueger, R. F. (1999). The structure of common mental disorders. Archives of General Psychiatry, 56(10), 921–926. https://doi.org/10.1001/archpsyc.56.10.921.CrossRefGoogle ScholarPubMed
Kujawa, A. J., Torpey, D., Kim, J., Hajcak, G., Rose, S., Gotlib, I. H., & Klein, D. N. (2011). Attentional biases for emotional faces in young children of mothers with chronic or recurrent depression. Journal of Abnormal Child Psychology, 39(1), 125–135. https://doi.org/10.1007/s10802-010-9438-6.CrossRefGoogle ScholarPubMed
Lang, P. J. (1995). The emotion probe: Studies of motivation and attention. The American Psychologist, 50(5), 372–385. https://doi.org/10.1037/0003-066x.50.5.372.CrossRefGoogle ScholarPubMed
Latzman, R. D., & DeYoung, C. G., & HiTOP Neurobiological Foundations Workgroup. (2020). Using empirically-derived dimensional phenotypes to accelerate clinical neuroscience: The hierarchical taxonomy of psychopathology (HiTOP) framework. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 45(7), 1083–1085. https://doi.org/10.1038/s41386-020-0639-6.CrossRefGoogle ScholarPubMed
Lewinsohn, P. M., Clarke, G. N., Seeley, J. R., & Rohde, P. (1994). Major depression in community adolescents: Age at onset, episode duration, and time to recurrence. Journal of the American Academy of Child and Adolescent Psychiatry, 33(6), 809–818. https://doi.org/10.1097/00004583-199407000-00006.CrossRefGoogle ScholarPubMed
MacNamara, A., & Barley, B. (2018). Event-related potentials to threat of predictable and unpredictable shock. Psychophysiology, 55(10), e13206. https://doi.org/10.1111/psyp.13206.CrossRefGoogle ScholarPubMed
Moffitt, T. E. (1993). Adolescence-limited and life-course-persistent antisocial behavior: A developmental taxonomy. Psychological Review, 100(4), 674–701. https://doi.org/10.1037/0033-295x.100.4.674.CrossRefGoogle ScholarPubMed
Muthén, B. O., du Toit, S. H. C., & Spisic, D. (1997). Robust interference using weighted least squares and quadratic estimating equations in the latent variable modeling with categorical and continuous outcomes. Unpublished Manuscript, Los Angeles, USA: University of California.Google Scholar
Nelson, B. D., & Hajcak, G. (2017a). Anxiety and depression symptom dimensions demonstrate unique relationships with the startle reflex in anticipation of unpredictable threat in 8 to 14 year-old girls. Journal of Abnormal Child Psychology, 45(2), 397–410. https://doi.org/10.1007/s10802-016-0169-1.CrossRefGoogle ScholarPubMed
Nelson, B. D., & Hajcak, G. (2017b). Defensive motivation and attention in anticipation of different types of predictable and unpredictable threat: A startle and event-related potential investigation. Psychophysiology, 54(8), 1180–1194. https://doi.org/10.1111/psyp.12869.CrossRefGoogle ScholarPubMed
Nelson, B. D., Hajcak, G., & Shankman, S. A. (2015). Event-related potentials to acoustic startle probes during the anticipation of predictable and unpredictable threat. Psychophysiology, 52(7), 887–894. https://doi.org/10.1111/psyp.12418.CrossRefGoogle ScholarPubMed
Nelson, B. D., McGowan, S. K., Sarapas, C., Robison-Andrew, E. J., Altman, S. E., Campbell, M. L., … Shankman, S. A. (2013). Biomarkers of threat and reward sensitivity demonstrate unique associations with risk for psychopathology. Journal of Abnormal Psychology, 122(3), 662–671. https://doi.org/10.1037/a0033982.CrossRefGoogle ScholarPubMed
Patrick, C. J., Bernat, E. M., Malone, S. M., Iacono, W. G., Krueger, R. F., & McGue, M. (2006). P300 amplitude as an indicator of externalizing in adolescent males. Psychophysiology, 43(1), 84–92. https://doi.org/10.1111/j.1469-8986.2006.00376.x.CrossRefGoogle ScholarPubMed
Paulus, M. P., & Thompson, W. K. (2019). The challenges and opportunities of small effects: The new normal in academic psychiatry. JAMA Psychiatry, 76(4), 353–354. https://doi.org/10.1001/jamapsychiatry.2018.4540.CrossRefGoogle ScholarPubMed
Peckham, A. D., McHugh, R. K., & Otto, M. W. (2010). A meta-analysis of the magnitude of biased attention in depression. Depression and Anxiety, 27(12), 1135–1142. https://doi.org/10.1002/da.20755.CrossRefGoogle ScholarPubMed
Robinson, O. J., Overstreet, C., Letkiewicz, A., & Grillon, C. (2012). Depressed mood enhances anxiety to unpredictable threat. Psychological Medicine, 42(7), 1397–1407. https://doi.org/10.1017/S0033291711002583.CrossRefGoogle ScholarPubMed
Sanislow, C. A., Pine, D. S., Quinn, K. J., Kozak, M. J., Garvey, M. A., Heinssen, R. K., … Cuthbert, B. N. (2010). Developing constructs for psychopathology research: Research domain criteria. Journal of Abnormal Psychology, 119(4), 631–639. https://doi.org/10.1037/a0020909.CrossRefGoogle ScholarPubMed
Schmitz, A., & Grillon, C. (2012). Assessing fear and anxiety in humans using the threat of predictable and unpredictable aversive events (the NPU-threat test). Nature Protocols, 7(3), 527–532. https://doi.org/10.1038/nprot.2012.001.CrossRefGoogle ScholarPubMed
Shankman, S. A., Robison-Andrew, E. J., Nelson, B. D., Altman, S. E., & Campbell, M. L. (2011). Effects of predictability of shock timing and intensity on aversive responses. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology, 80(2), 112–118. https://doi.org/10.1016/j.ijpsycho.2011.02.008.CrossRefGoogle ScholarPubMed
Steiger, J. H. (1990). Structural model evaluation and modification: An interval estimation approach. Multivariate Behavioral Research, 25(2), 173–180. https://doi.org/10.1207/s15327906mbr2502_4.CrossRefGoogle ScholarPubMed
Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., … Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168(3), 242–249. https://doi.org/10.1016/j.psychres.2008.05.006.CrossRefGoogle ScholarPubMed
Tucker, L. R., & Lewis, C. (1973). A reliability coefficient for maximum likelihood factor analysis. Psychometrika, 38(1), 1–10. https://doi.org/10.1007/bf02291170.CrossRefGoogle Scholar
Watson, D. (2005). Rethinking the mood and anxiety disorders: A quantitative hierarchical model for DSM-V. Journal of Abnormal Psychology, 114(4), 522–536. https://doi.org/10.1037/0021-843x.114.4.522.CrossRefGoogle ScholarPubMed
Supplementary material: File

Beatty et al. supplementary material

Beatty et al. supplementary material

Download Beatty et al. supplementary material(File)
File 19.1 KB