Skip to main content
SpringerLink
Log in

Extinction Learning as a Potential Mechanism Linking High Vagal Tone with Lower PTSD Symptoms among Abused Youth

  • Published:
Journal of Abnormal Child Psychology Aims and scope Submit manuscript

Abstract

Childhood abuse is a potent risk factor for psychopathology, including posttraumatic stress disorder (PTSD). Research has shown high resting vagal tone, a measure of parasympathetic nervous system function, protects abused youth from developing internalizing psychopathology, but potential mechanisms explaining this effect are unknown. We explored fear extinction learning as a possible mechanism underlying the protective effect of vagal tone on PTSD symptoms among abused youth. We measured resting respiratory sinus arrhythmia (RSA) and skin conductance responses (SCR) during a fear conditioning and extinction task in youth with variability in abuse exposure (N = 94; aged 6–18 years). High RSA predicted lower PTSD symptoms and enhanced extinction learning among abused youths. In a moderated-mediation model, extinction learning mediated the association of abuse with PTSD symptoms only among youth with high RSA. These findings highlight extinction learning as a possible mechanism linking high vagal tone to decreased risk for PTSD symptoms among abused youth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allen, J. J., Chambers, A. S., & Towers, D. N. (2007). The many metrics of cardiac chronotropy: A pragmatic primer and a brief comparison of metrics. Biological Psychology, 74(2), 243–262.

    Article  Google Scholar 

  • Asmundson, G. J. G., & Stapleton, J. A. (2008). Associations between dimensions of anxiety sensitivity and PTSD symptom clusters in active-duty police officers. Cognitive Behaviour Therapy, 37, 66–75. https://doi.org/10.1080/16506070801969005.

    Article  PubMed  Google Scholar 

  • Bauer, D. J., & Curran, P. J. (2005). Probing interactions in fixed and multilevel regression: Inferential and graphical techniques. Multivariate behavioral research, 40(3), 373–400.

  • Beauchaine, T. (2001). Vagal tone, development, and Gray’s motivational theory: Toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13(02), 183–214.

    Article  Google Scholar 

  • Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135(6), 885–908.

    Article  Google Scholar 

  • Bernstein, D. P., Ahluvalia, T., Pogge, D., & Handelsman, L. (1997). Validity of the childhood trauma questionnaire in an adolescent psychiatric population. Journal of the American Academy of Child & Adolescent Psychiatry, 36(3), 340–348.

    Article  Google Scholar 

  • Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1993). Respiratory sinus arrhythmia: Autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology, 30(2), 183–196.

    Article  Google Scholar 

  • Berntson, G G, Bigger, J. T., Jr, 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(6), 623–648.

  • Bifulco, A., Brown, G. W., & Harris, T. O. (1994). Childhood experience of care and abuse (CECA): A retrospective interview measure. Journal of Child Psychology and Psychiatry, 35(8), 1419–1435.

    Article  Google Scholar 

  • Busso, D. S., McLaughlin, K. A., & Sheridan, M. A. (2014). MEDIA EXPOSURE AND SYMPATHETIC NERVOUS SYSTEM REACTIVITY PREDICT PTSD SYMPTOMS AFTER THE BOSTON MARATHON BOMBINGS: Research article: Vulnerability to PTSD symptoms following a terrorist attack. Depression and Anxiety, 31(7), 551–558. https://doi.org/10.1002/da.22282.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cacioppo, J. T., Tassinary, L. G., & Berntson, G. (2007). Handbook of psychophysiology. Cambridge University Press.

  • Calkins, S. D., & Keane, S. P. (2004). Cardiac vagal regulation across the preschool period: Stability, continuity, and implications for childhood adjustment. Developmental Psychobiology, 45(3), 101–112.

    Article  Google Scholar 

  • Calkins, S. D., Graziano, P. A., & Keane, S. P. (2007). Cardiac vagal regulation differentiates among children at risk for behavior problems. Biological Psychology, 74(2), 144–153.

    Article  Google Scholar 

  • Childs, J. E., DeLeon, J., Nickel, E., & Kroener, S. (2017). Vagus nerve stimulation reduces cocaine seeking and alters plasticity in the extinction network. Learning & Memory, 24(1), 35–42.

    Article  Google Scholar 

  • Daban, C., Martinez-Aran, A., Cruz, N., & Vieta, E. (2008). Safety and efficacy of Vagus nerve stimulation in treatment-resistant depression. A systematic review. Journal of Affective Disorders, 110(1), 1–15.

    Article  Google Scholar 

  • Dawson, M. E., Schell, A. M., & Filion, D. L. (2007). The electrodermal system. Handbook of Psychophysiology, 2, 200–223.

    Google Scholar 

  • Descilo, T., Vedamurtachar, A., Gerbarg, P. L., Nagaraja, D., Gangadhar, B. N., Damodaran, B., Adelson, B., Braslow, L. H., Marcus, S., & Brown, R. P. (2010). Effects of a yoga breath intervention alone and in combination with an exposure therapy for post-traumatic stress disorder and depression in survivors of the 2004 South-East Asia tsunami. Acta Psychiatrica Scandinavica, 121(4), 289–300.

    Article  Google Scholar 

  • Ditto, B., Eclache, M., & Goldman, N. (2006). Short-term autonomic and cardiovascular effects of mindfulness body scan meditation. Annals of Behavioral Medicine, 32(3), 227–234. https://doi.org/10.1207/s15324796abm3203_9.

    Article  PubMed  Google Scholar 

  • Dorsey, S., Briggs, E. C., & Woods, B. A. (2011). Cognitive-behavioral treatment for posttraumatic stress disorder in children and adolescents. Child and Adolescent Psychiatric Clinics of North America, 20(2), 255–269.

    Article  Google Scholar 

  • Eisenberg, N., Fabes, R. A., Murphy, B., Maszk, P., Smith, M., & Karbon, M. (1995). The role of emotionality and regulation in Children’s social functioning: A longitudinal study. Child Development, 66(5), 1360–1384. https://doi.org/10.1111/j.1467-8624.1995.tb00940.x.

    Article  PubMed  Google Scholar 

  • El-Sheikh, M., & Whitson, S. A. (2006). Longitudinal relations between marital conflict and child adjustment: Vagal regulation as a protective factor. Journal of Family Psychology, 20(1), 30–39.

    Article  Google Scholar 

  • El-Sheikh, M., Harger, J., & Whitson, S. M. (2001). Exposure to interparental conflict and children’s adjustment and physical health: The moderating role of vagal tone. Child Development, 72(6), 1617–1636.

    Article  Google Scholar 

  • Fabes, R. A., Eisenberg, N., & Eisenbud, L. (1993). Behavioral and physiological correlates of children’s reactions to others in distress. Developmental Psychology, 29(4), 655–663. https://doi.org/10.1037/0012-1649.29.4.655.

    Article  Google Scholar 

  • Friedman, B. H. (2007). An autonomic flexibility–neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology, 74(2), 185–199.

    Article  Google Scholar 

  • Glover, E. M., Phifer, J. E., Crain, D. F., Norrholm, S. D., Davis, M., Bradley, B., Ressler, K. J., & Jovanovic, T. (2011). Tools for translational neuroscience: PTSD is associated with heightened fear responses using acoustic startle but not skin conductance measures. Depression and Anxiety, 28(12), 1058–1066. https://doi.org/10.1002/da.20880.

    Article  PubMed  Google Scholar 

  • Guthrie, R. M., & Bryant, R. A. (2005). Auditory startle response in firefighters before and after trauma exposure. American Journal of Psychiatry, 162(2), 283–290.

    Article  Google Scholar 

  • Hayes, A. F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: Guilford Press.

    Google Scholar 

  • Katz, L. F., & Gottman, J. M. (1995). Vagal tone protects children from marital conflict. Development and Psychopathology, 7(1), 83–92.

    Article  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(1), 213–222.

    Article  Google Scholar 

  • LeDoux, J. E. (2014). Coming to terms with fear. Proceedings of the National Academy of Sciences, 111(8), 2871–2878. https://doi.org/10.1073/pnas.1400335111.

    Article  Google Scholar 

  • Liu, J., Fang, J., Wang, Z., Rong, P., Hong, Y., Fan, Y., … others. (2016). Transcutaneous vagus nerve stimulation modulates amygdala functional connectivity in patients with depression. Journal of Affective Disorders, 205, 319–326.

  • Lucini, D., Di Fede, G., Parati, G., & Pagani, M. (2005). Impact of chronic psychosocial stress on autonomic cardiovascular regulation in otherwise healthy subjects. Hypertension, 46(5), 1201–1206.

    Article  Google Scholar 

  • McLaughlin, K. A., & Sheridan, M. A. (2016). Beyond cumulative risk: A dimensional approach to childhood adversity. Current Directions in Psychological Science, 25(4), 239–245.

    Article  Google Scholar 

  • McLaughlin, K. A., Green, J. G., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2012). Childhood adversities and first onset of psychiatric disorders in a national sample of US adolescents. Archives of General Psychiatry, 69(11), 1151–1160.

    Article  Google Scholar 

  • McLaughlin, K. A., Koenen, K. C., Hill, E. D., Petukhova, M., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2013). Trauma exposure and posttraumatic stress disorder in a national sample of adolescents. Journal of the American Academy of Child & Adolescent Psychiatry, 52(8), 815–830.

    Article  Google Scholar 

  • McLaughlin, K. A., Alves, S., & Sheridan, M. A. (2014a). Vagal regulation and internalizing psychopathology among adolescents exposed to childhood adversity. Developmental Psychobiology, 56(5), 1036–1051.

    Article  Google Scholar 

  • McLaughlin, K. A., Sheridan, M. A., & Lambert, H. K. (2014b). Childhood adversity and neural development: Deprivation and threat as distinct dimensions of early experience. Neuroscience & Biobehavioral Reviews, 47, 578–591.

    Article  Google 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 & Adolescent Psychology, 44(2), 314–328.

    Article  Google Scholar 

  • McLaughlin, K. A., Sheridan, M. A., Gold, A. L., Duys, A., Lambert, H. K., Peverill, M., Heleniak, C., Shechner, T., Wojcieszak, Z., & Pine, D. S. (2016). Maltreatment exposure, brain structure, and fear conditioning in children and adolescents. Neuropsychopharmacology Retrieved from http://www.nature.com/npp/journal/vaop/ncurrent/full/npp2015365a.html , 41, 1956–1964.

    Article  Google Scholar 

  • Mezzacappa, E., Kindlon, D., Saul, J. P., & Earls, F. (1998). Executive and motivational control of performance task behavior, and autonomic heart-rate regulation in children: Physiologic validation of two-factor solution inhibitory control. Journal of Child Psychology and Psychiatry, 39(4), 525–531.

    Article  Google Scholar 

  • Milad, M. R., & Quirk, G. J. (2002). Neurons in medial prefrontal cortex signal memory for fear extinction. Nature, 420(6911), 70–74.

    Article  Google Scholar 

  • Milad, M. R., & Quirk, G. J. (2012). Fear extinction as a model for translational neuroscience: Ten years of progress. Annual Review of Psychology, 63, 129–151.

    Article  Google Scholar 

  • Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., Zeidan, M. A., Handwerger, K., Orr, S. P., & Rauch, S. L. (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry, 66(12), 1075–1082. https://doi.org/10.1016/j.biopsych.2009.06.026.

    Article  PubMed  PubMed Central  Google Scholar 

  • Neumann, S. A., Brown, S. M., Ferrell, R. E., Flory, J. D., Manuck, S. B., & Hariri, A. R. (2006). Human choline transporter gene variation is associated with corticolimbic reactivity and autonomic-cholinergic function. Biological Psychiatry, 60(10), 1155–1162.

    Article  Google Scholar 

  • Peña, D. F., Engineer, N. D., & McIntyre, C. K. (2013). Rapid remission of conditioned fear expression with extinction training paired with vagus nerve stimulation. Biological Psychiatry, 73(11), 1071–1077.

    Article  Google Scholar 

  • Peña, D. F., Childs, J. E., Willett, S., Vital, A., McIntyre, C. K., & Kroener, S. (2014). Vagus nerve stimulation enhances extinction of conditioned fear and modulates plasticity in the pathway from the ventromedial prefrontal cortex to the amygdala. Frontiers in Behavioral Neuroscience, 8 Retrieved from https://books.google.com/books?hl=en&lr=&id=-wXmCgAAQBAJ&oi=fnd&pg=PA60&dq=pena+vagal+tone+rats&ots=ZDA8DNWquX&sig=GhM0KKKQmGQf9BX4G9Q6_zsVGH0.

  • Pine, D. S., Wasserman, G. A., Miller, L., Coplan, J. D., Bagiella, E., Kovelenku, P., et al. (1998). Heart period variability and psychopathology in urban boys at risk for delinquency. Psychophysiology, 35(5), 521–529.

    Article  Google Scholar 

  • Pole, N., Neylan, T. C., Otte, C., Henn-Hasse, C., Metzler, T. J., & Marmar, C. R. (2009). Prospective prediction of posttraumatic stress disorder symptoms using fear potentiated auditory startle responses. Biological Psychiatry, 65(3), 235–240.

    Article  Google Scholar 

  • Porges, S. W. (1995). Orienting in a defensive world: Mammalian modifications of our evolutionary heritage. A polyvagal theory. Psychophysiology, 32(4), 301–318.

    Article  Google Scholar 

  • Porges, S. W. (2007). The polyvagal perspective. Biological Psychology, 74(2), 116–143.

    Article  Google Scholar 

  • Raine, A. (1996). Autonomic nervous system factors underlying disinhibited, antisocial, and violent behavior biosocial perspectives and treatment implications. Annals of the New York Academy of Sciences, 794(1), 46–59.

    Article  Google Scholar 

  • Shannon, K. E., Beauchaine, T. P., Brenner, S. L., Neuhaus, E., & Gatzke-Kopp, L. (2007). Familial and temperamental predictors of resilience in children at risk for conduct disorder and depression. Development and Psychopathology, 19(03), 701–727.

    Article  Google Scholar 

  • Shechner, T., Britton, J. C., Ronkin, E. G., Jarcho, J. M., Mash, J. A., Michalska, K. J., Leibenluft, E., & Pine, D. S. (2015). Fear conditioning and extinction in anxious and nonanxious youth and adults: Examining a novel developmentally appropriate fear-conditioning task. Depression and Anxiety, 32(4), 277–288. https://doi.org/10.1002/da.22318.

    Article  PubMed  Google Scholar 

  • Sherwood, A., Allen, M. T., Fahrenberg, J., Kelsey, R. M., Lovallo, W. R., & van Doornen, L. J. P. (1990). Methodological guidelines for impedance Cardiography. Psychophysiology, 27(1), 1–23. https://doi.org/10.1111/j.1469-8986.1990.tb02171.x.

    Article  PubMed  Google Scholar 

  • Steinberg, A. M., Brymer, M. J., Decker, K. B., & Pynoos, R. S. (2004). The University of California at Los Angeles post-traumatic stress disorder reaction index. Current Psychiatry Reports, 6(2), 96–100.

    Article  Google Scholar 

  • Steinberg, A. M., Brymer, M. J., Kim, S., Briggs, E. C., Ippen, C. G., Ostrowski, S. A., Gully, K. J., & Pynoos, R. S. (2013). Psychometric properties of the UCLA PTSD reaction index: Part I. Journal of Traumatic Stress, 26(1), 1–9. https://doi.org/10.1002/jts.21780.

    Article  PubMed  Google Scholar 

  • Stewart, S. H., Conrod, P. J., Pihl, R. O., & Dongier, M. (1999). Relations between posttraumatic stress symptom dimensions and substance dependence in a community-recruited sample of substance-abusing women. Psychology of Addictive Behaviors, 13(2), 78–88. https://doi.org/10.1037/0893-164X.13.2.78.

    Article  Google Scholar 

  • Thayer, J. F., Ahs, 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 & Biobehavioral Reviews, 36(2), 747–756.

    Article  Google Scholar 

  • Vouimba, R.-M., & Maroun, M. (2011). Learning-induced changes in mPFC–BLA connections after fear conditioning, extinction, and reinstatement of fear. Neuropsychopharmacology, 36(11), 2276–2285.

    Article  Google Scholar 

  • Walker, E. A., Unutzer, J., Rutter, C., Gelfand, A., Saunders, K., VonKorff, M., & Katon, W. (1999). Costs of health care use by women HMO members with a history of childhood abuse and neglect. Archives of General Psychiatry, 56(7), 609–613.

  • Widom, C. S., Weiler, B. L., & Cottler, L. B. (1999). Childhood victimization and drug abuse: A comparison of prospective and retrospective findings. Journal of consulting and clinical psychology, 67(6), 867.

Download references

Acknowledgments

This research was supported by the Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32 HD057822-06: JLJ; F32 HD089514: MLR), the National Institute of Mental Health (R01-MH103291: KAM; F32 MH108238: ABM; K23MH112872-01: JLJ), a Brain and Behavior Research Foundation NARSAD Young Investigator Grant (KAM), and a Jacobs Foundation Early Career Research Fellowship (KAM).

Author information

Authors and Affiliations

  1. Department of Psychiatry and Behavioral Sciences, University of Washington, 6200 NE 74th St., Seattle, WA, 98115, USA

    Jessica L. Jenness

  2. Department of Psychology and Neuroscience, University of North Carolina, 235 E, Ave. Chapel Hill, Cameron, NC, 27599, USA

    Adam Bryant Miller

  3. Department of Psychology, University of Washington, Seattle, WA, USA

    Maya L. Rosen

  4. Department of Psychology, Harvard University, Boston, MA, USA

    Katie A. McLaughlin

Authors
  1. Jessica L. Jenness
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam Bryant Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maya L. Rosen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Katie A. McLaughlin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katie A. McLaughlin.

Ethics declarations

Conflict of Interest

The authors have no conflicts of interest to disclose.

Ethical Approval

All procedures were approved by the Institutional Review Board at the University of Washington and performed in accordance with the ethical standards as outlined in the 1964 Declaration of Helsinki.

Informed Consent

Youth completed questionnaire measures to assess for PTSD symptomatology. Informed consent was obtained from the parent or guardian who attended the session with the participant, and assent was provided by all youth participants.

Electronic supplementary material

Supplemental Table 1

(DOCX 15 kb)

Supplemental Table 2

(DOCX 62 kb)

Supplemental Fig. 1

Fear conditioning task (JPG 68 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jenness, J.L., Miller, A.B., Rosen, M.L. et al. Extinction Learning as a Potential Mechanism Linking High Vagal Tone with Lower PTSD Symptoms among Abused Youth. J Abnorm Child Psychol 47, 659–670 (2019). https://doi.org/10.1007/s10802-018-0464-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10802-018-0464-0

Keywords

Search

Navigation