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07-01-2021 | Original Article

Inhibitory Control Moderates the Effect of Anxiety on Vagally Mediated Heart Rate Variability: Findings from a Community Sample of Young School-Aged Children

Auteurs: Tonje Grønning Andersen, Charlotte Fiskum, Karl Henry Jacobsen, Stian Lydersen, Lars Wichstrøm

Gepubliceerd in: Cognitive Therapy and Research | Uitgave 4/2021

Abstract

Background

Individuals with anxiety disorders show both excessive and blunted vagally mediated heart rate variability (vmHRV) reactivity to stress. Scholars have suggested that differences in cognitive control could explain such heterogeneity, but this proposition has not been tested. The present study hence investigated the moderating effect of executive functions, particularly inhibitory control, on the relationship between anxiety symptoms and vmHRV reactivity.

Methods

We evaluated anxiety symptoms (a diagnostic interview with parents) and executive functions (parent-reported questionnaire) in 262 six-year-olds from a community sample. vmHRV responses to neutral tasks and stressors were analyzed using latent growth curve modeling.

Results

Results supported a moderating effect of inhibitory control; children with more anxiety symptoms and enhanced inhibitory control showed a blunted decrease in vmHRV in response to stressors. In contrast, counterparts with impaired inhibitory control evinced an excessive decrease in vmHRV. Children with no anxiety symptoms did not differ in vmHRV reactivity, independent of the level of inhibitory control.

Conclusions

The results could indicate that anxious children with enhanced inhibitory control successfully utilized a cognitive avoidance strategy (i.e. verbal worry) to inhibit expected autonomic arousal in response to threat. Clinical implications are discussed.

vorige artikel Examining the associations between interpersonal emotion regulation and psychosocial adjustment in emerging adulthood

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Al’Absi, M., Bongard, S., Buchanan, T., Pincomb, G. A., Licinio, J., & Lovallo, W. R. (1997). Cardiovascular and neuroendocrine adjustment to public speaking and mental arithmetic stressors. Psychophysiology, 34(3), 266–275. https://doi.org/10.1111/j.1469-8986.1997.tb02397.x.CrossRefPubMed

Alkon, A., Goldstein, L. H., Smider, N., Essex, M. J., Kupfer, D. J., & Boyce, W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42(1), 64–78. https://doi.org/10.1002/dev.10082.CrossRefPubMed

Allen, J. J. B., 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. https://doi.org/10.1016/j.biopsycho.2006.08.005.CrossRefPubMed

Andersen, T. G., Fiskum, C., Aslaksen, P. M., Flaten, M. A., & Jacobsen, K. H. (2020). Internalizing Problems and Attentional Control: Effects on Cardiac Autonomic Responses After the Induction of Negative Affect. Journal of Psychophysiology, 34(2), 110–122. https://doi.org/10.1027/0269-8803/a000241.CrossRef

Barkley, R. A. (1997). Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychological Bulletin, 121(1), 65–94. https://doi.org/10.1037/0033-2909.121.1.65.CrossRefPubMed

Barrett, L. F. (2009). Variety is the spice of life: A psychological construction approach to understanding variability in emotion. Cognition and Emotion, 23(7), 1284–1306. https://doi.org/10.1080/02699930902985894.CrossRefPubMed

Beauchaine, T. P. (2001). Vagal tone, development, and Gray’s motivational theory: Toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13(2), 183–214. https://doi.org/10.1017/S0954579401002012.CrossRefPubMed

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, 56, e13329. https://doi.org/10.1111/psyp.13329.CrossRefPubMedPubMedCentral

Bodnar, L. E., Prahme, M. C., Cutting, L. E., Denckla, M. B., & Mahone, E. M. (2007). Construct validity of parent ratings of inhibitory control. Child Neuropsychology, 13(4), 345–362. https://doi.org/10.1080/09297040600899867.CrossRefPubMed

Bögels, S. M., & Zigterman, D. (2000). Dysfunctional cognitions in children with social phobia, separation anxiety disorder, and generalized anxiety disorder. Journal of Abnormal Child Psychology, 28(2), 205–211. https://doi.org/10.1023/A:1005179032470.CrossRefPubMed

Borkovec, T. D., Lyonfields, J. D., Wiser, S. L., & Deihl, L. (1993). The role of worrisome thinking in the suppression of cardiovascular response to phobic imagery. Behaviour Research and Therapy, 31(3), 321–324. https://doi.org/10.1016/0005-7967(93)90031-O.CrossRefPubMed

Borkovec, T. D., Ray, W. J., & Stöber, J. (1998). Worry: A cognitive phenomenon intimately linked to affective, physiological, and interpersonal behavioral processes. Cognitive Therapy and Research, 22(6), 561–576. https://doi.org/10.1023/A:1018790003416.CrossRef

Boyce, W. T., Quas, J., Alkon, A., Smider, N. A., Essex, M. J., & Kupfer, D. J. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry, 179, 144–150. https://doi.org/10.1192/bjp.179.2.144.CrossRef

Busscher, B., Spinhoven, P., & de Geus, E. J. C. (2015). Psychological distress and physiological reactivity during in vivo exposure in people with aviophobia. Psychosomatic Medicine, 77(7), 762–774. https://doi.org/10.1097/PSY.0000000000000209.CrossRefPubMed

Costello, E. J., Mustillo, S., Erkanli, A., Keeler, G., & Angold, A. (2003). Prevalence and development of psychiatric disorders in childhood and adolescence. Archives of General Psychiatry, 60(8), 837–844. https://doi.org/10.1001/archpsyc.60.8.837.CrossRefPubMed

Derryberry, D., & Reed, M. A. (2002). Anxiety-related attentional biases and their regulation by attentional control. Journal of Abnormal Psychology, 111(2), 225–236. https://doi.org/10.1037/0021-843X.111.2.225.CrossRefPubMed

Edelmann, R. J., & Baker, S. R. (2002). Self-reported and actual physiological responses in social phobia. British Journal of Clinical Psychology, 41(1), 1–14. https://doi.org/10.1348/014466502163732.CrossRefPubMed

Egger, H. L., Erkanli, A., Keeler, G., Potts, E., Walter, B. K., & Angold, A. (2006). Test-retest reliability of the preschool age psychiatric assessment (PAPA). Journal of the American Academy of Child & Adolescent Psychiatry, 45(5), 538–549. https://doi.org/10.1097/01.chi.0000205705.71194.b8.CrossRef

Eisenberg, N., Hofer, C., Sulik, M. J., & Spinrad, T. L. (2014). Self-regulation, effortful control, and their socioemotional correlates. In J. J. Gross (Ed.), Handbook of emotion regulation (2 ed., p. 157–172). New York: The Guilford Press.

Eisenberg, N., & Zhou, Q. (2016). Conceptions of executive function and regulation: When and to what degree do they overlap? In J. A. Griffin, P. McCardle, & L. S. Freund (Eds.), Executive function in preschool-age children. Integrating measurement, neurodevelopment, and translational research (p. 115–136). Washington, DC: American Psychological Association.CrossRef

Ellenbogen, M. A., & Schwartzman, A. E. (2009). Selective attention and avoidance on a pictorial cueing task during stress in clinically anxious and depressed participants. Behaviour Research and Therapy, 47(2), 128–138. https://doi.org/10.1016/j.brat.2008.10.021.CrossRefPubMed

Etkin, A., Prater, K. E., Schatzberg, A. F., Menon, V., & Greicius, M. D. (2009). Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Archives of General Psychiatry, 66(12), 1361–1372. https://doi.org/10.1001/archgenpsychiatry.2009.104.CrossRefPubMed

Fishback, G. M., Chriki, L., Thayer, J. F., & Vasey, M. W. (2020). Heart rate variability moderates the association between beliefs about worry and generalized anxiety disorder symptoms. Frontiers in Neuroscience, 14, 569359. https://doi.org/10.3389/fnins.2020.569359.CrossRefPubMedPubMedCentral

Fiskum, C. (2019). Psychotherapy beyond all the words: Dyadic expansion, vagal regulation, and biofeedback in psychotherapy. Journal of Psychotherapy Integration, 29(4), 412–425. https://doi.org/10.1037/int0000174.CrossRef

Fonzo, G. A., & Etkin, A. (2016). Brain connectivity reflects mental and physical states in generalized anxiety disorder. Biological Psychiatry, 80(10), 733–735. https://doi.org/10.1016/j.biopsych.2016.08.026.CrossRefPubMed

de Geus, E. J. C., Gianaros, P. J., Brindle, R. C., Jennings, J. R., & Berntson, G. G. (2019). Should heart rate variability be “corrected” for heart rate? Biological, quantitative, and interpretive considerations. Psychophysiology, 56(2), e13287. https://doi.org/10.1111/psyp.13287.CrossRefPubMed

Gioia, G. A., Isquith, P. K., Retzlaff, P. D., & Espy, K. A. (2002). Confirmatory factor analysis of the Behavior Rating Inventory of Executive Function (BRIEF) in a clinical sample. Child Neuropsychology, 8(4), 249–257. https://doi.org/10.1076/chin.8.4.249.13513.CrossRefPubMed

Goedhart, A. D., van der Sluis, S., Houtveen, J. H., Willemsen, G., & de Geus, E. J. C. (2007). Comparison of time and frequency domain measures of RSA in ambulatory recordings. Psychophysiology, 44(2), 203–215. https://doi.org/10.1111/j.1469-8986.2006.00490.x.CrossRefPubMed

Graziano, P., & Derefinko, K. (2013). Cardiac vagal control and children’s adaptive functioning: A meta-analysis. Biological Psychology, 94(1), 22–37. https://doi.org/10.1016/j.biopsycho.2013.04.011.CrossRefPubMedPubMedCentral

Grossman, P., & Taylor, E. W. (2007). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology, 74(2), 263–285. https://doi.org/10.1016/j.biopsycho.2005.11.014.CrossRefPubMed

Hallion, L. S., Tolin, D. F., & Diefenbach, G. J. (2019). Enhanced cognitive control over task-irrelevant emotional distractors in generalized anxiety disorder versus obsessive-compulsive disorder. Journal of Anxiety Disorders, 64, 71–78. https://doi.org/10.1016/j.janxdis.2019.02.004.CrossRefPubMed

Halvorsen, M., Mathiassen, B., Amundsen, T., Ellingsen, J., Brøndbo, P. H., Sundby, J., et al. (2019). Confirmatory factor analysis of the behavior rating inventory of executive function in a neuro-pediatric sample and its application to mental disorders. Child Neuropsychology, 25(5), 599–616. https://doi.org/10.1080/09297049.2018.1508564.

Heatherton, T. F., & Wagner, D. D. (2011). Cognitive neuroscience of self-regulation failure. Trends in Cognitive Sciences, 15(3), 132–139. https://doi.org/10.1016/j.tics.2010.12.005.CrossRefPubMedPubMedCentral

Hirsch, C. R., & Mathews, A. (2012). A cognitive model of pathological worry. Behaviour Research and Therapy, 50(10), 636–646. https://doi.org/10.1016/j.brat.2012.06.007.CrossRefPubMedPubMedCentral

Hofmann, S. G., Moscovitch, D. A., Litz, B. T., Kim, H.-J., Davis, L. L., & Pizzagalli, D. A. (2005). The worried mind: autonomic and prefrontal activation during worrying. Emotion, 5(4), 464–475. https://doi.org/10.1037/1528-3542.5.4.464.CrossRefPubMed

Hummer, T. A., Kronenberger, W. G., Wang, Y., Dunn, D. W., Mosier, K. M., Kalnin, A. J., & Mathews, V. P. (2011). Executive functioning characteristics associated with ADHD comorbidity in adolescents with disruptive behavior disorders. Journal of Abnormal Child Psychology, 39, 11–19. https://doi.org/10.1007/s10802-010-9449-3.CrossRefPubMed

Keeton, C. P., Kolos, A. C., & Walkup, J. T. (2009). Pediatric Generalized Anxiety Disorder. Pediatric Drugs, 11(3), 171–183. https://doi.org/10.2165/00148581-200911030-00003.CrossRefPubMed

Kendall, P. C., Compton, S. N., Walkup, J. T., Birmaher, B., Albano, A. M., Sherrill, J., et al. (2010). Clinical characteristics of anxiety disordered youth. Journal of Anxiety Disorders, 24(3), 360–365. https://doi.org/10.1016/j.janxdis.2010.01.009.

Koenig, J., Rash, J. A., Campbell, T. S., Thayer, J. F., & Kaess, M. (2017). A meta-analysis on sex differences in resting-state vagal activity in children and adolescents. Frontiers in Physiology, 8, 582. https://doi.org/10.3389/fphys.2017.00582.CrossRefPubMedPubMedCentral

Kreibig, S. D. (2010). Autonomic nervous system activity in emotion: A review. Biological Psychology, 84(3), 394–421. https://doi.org/10.1016/j.biopsycho.2010.03.010.CrossRefPubMed

Leigh, E., & Hirsch, C. R. (2011). Worry in imagery and verbal form: Effect on residual working memory capacity. Behaviour Research and Therapy, 49(2), 99–105. https://doi.org/10.1016/j.brat.2010.11.005.CrossRefPubMedPubMedCentral

Levine, J. C., Fleming, R., Piedmont, J. I., Cain, S. M., & Chen, W.-J. (2016). Heart rate variability and generalized anxiety disorder during laboratory-induced worry and aversive imagery. Journal of Affective Disorders, 205, 207–215. https://doi.org/10.1016/j.jad.2016.07.019.CrossRefPubMed

Lindquist, K. A., & Barrett, L. F. (2012). A functional architecture of the human brain: emerging insights from the science of emotion. Trends in Cognitive Sciences, 16(11), 533–540. https://doi.org/10.1016/j.tics.2012.09.005.CrossRefPubMedPubMedCentral

Makovac, E., Meeten, F., Watson, D. R., Herman, A., Garfinkel, S. N., Critchley, H. D., & Ottaviani, C. (2016). Alterations in amygdala-prefrontal functional connectivity account for excessive worry and autonomic dysregulation in generalized anxiety disorder. Biological Psychiatry, 80(10), 786–795. https://doi.org/10.1016/j.biopsych.2015.10.013.CrossRefPubMed

Mauss, I., Wilhelm, F., & Gross, J. (2004). Is there less to social anxiety than meets the eye? Emotion experience, expression, and bodily responding. Cognition and Emotion, 18(5), 631–662. https://doi.org/10.1080/02699930341000112.CrossRef

Mogg, K., Bradley, B., Miles, F., & Dixon, R. (2004). BRIEF REPORT Time course of attentional bias for threat scenes: Testing the vigilance-avoidance hypothesis. Cognition and Emotion, 18(5), 689–700. https://doi.org/10.1080/02699930341000158.CrossRef

Mogg, K., & Bradley, B. P. (2005). Attentional bias in generalized anxiety disorder versus depressive disorder. Cognitive Therapy and Research, 29, 29–45. https://doi.org/10.1007/s10608-005-1646-y.CrossRef

Newman, M. G., & Llera, S. J. (2011). A novel theory of experiential avoidance in generalized anxiety disorder: A review and synthesis of research supporting a contrast avoidance model of worry. Clinical Psychology Review, 31(3), 371–382. https://doi.org/10.1016/j.cpr.2011.01.008.CrossRefPubMedPubMedCentral

Nigg, J. T. (2017). Annual Research Review: On the relations among self-regulation, self-control, executive functioning, effortful control, cognitive control, impulsivity, risk-taking, and inhibition for developmental psychopathology. Journal of Child Psychology and Psychiatry, 58(4), 361–383. https://doi.org/10.1111/jcpp.12675.CrossRefPubMed

Penttilä, J., Helminen, A., Jartti, T., Kuusela, T., Huikuri, H. V., Tulppo, M. P., et al. (2001). Time domain, geometrical and frequency domain analysis of cardiac vagal outflow: effects of various respiratory patterns. Clinical Physiology, 21(3), 365–376. https://doi.org/10.1046/j.1365-2281.2001.00337.x.

Porges, S. W. (1995). Orienting in a defensive world: Mammalian modifications of our evolutionary heritage. A Polyvagal Theory. Psychophysiology, 32(4), 301–318. https://doi.org/10.1111/j.1469-8986.1995.tb01213.x.CrossRefPubMed

Roisman, G. I., Newman, D. A., Fraley, R. C., Haltigan, J. D., Groh, A. M., & Haydon, K. C. (2012). Distinguishing differential susceptibility from diathesis–stress: Recommendations for evaluating interaction effects. Development and Psychopathology, 24(2), 389–409. https://doi.org/10.1017/S0954579412000065.CrossRefPubMed

Schmitz, J., Krämer, M., Tuschen-Caffier, B., Heinrichs, N., & Blechert, J. (2011). Restricted autonomic flexibility in children with social phobia. Journal of Child Psychology and Psychiatry, 52(11), 1203–1211. https://doi.org/10.1111/j.1469-7610.2011.02417.x.CrossRefPubMed

Shader, T. M., Gatzke-Kopp, L. M., Crowell, S. E., Reid, M. J., Thayer, J. F., Vasey, M. W., et al. (2018). Quantifying respiratory sinus arrhythmia: Effects of misspecifying breathing frequencies across development. Development and Psychopathology, 30(1), 351–366. https://doi.org/10.1017/S0954579417000669.

Smith, R., Thayer, J. F., Khalsa, S. S., & Lane, R. D. (2017). The hierarchical basis of neurovisceral integration. Neuroscience & Biobehavioral Reviews, 75, 274–296. https://doi.org/10.1016/j.neubiorev.2017.02.003.CrossRef

Steinsbekk, S., & Wichstrøm, L. (2018). Cohort Profile: The Trondheim Early Secure Study (TESS)—a study of mental health, psychosocial development and health behaviour from preschool to adolescence. International Journal of Epidemiology, 47(5), 1401–1401i. https://doi.org/10.1093/ije/dyy190.CrossRefPubMed

Stokes, C., & Hirsch, C. R. (2010). Engaging in imagery versus verbal processing of worry: Impact on negative intrusions in high worriers. Behaviour Research and Therapy, 48(5), 418–423. https://doi.org/10.1016/j.brat.2009.12.011.CrossRefPubMedPubMedCentral

Sulik, M. J., Eisenberg, N., Silva, K. M., Spinrad, T. L., & Kupfer, A. (2013). Respiratory sinus arrhythmia, shyness, and effortful control in preschool-age children. Biological Psychology, 92(2), 241–248. https://doi.org/10.1016/j.biopsycho.2012.10.009.CrossRefPubMed

Tarvainen, M. P., Lipponen, J., Niskanen, J.-P., & Ranta-aho, P. O. (2018). Kubios HRV (ver. 3.1.) User’s guide. Techn. Ber., Kubios Oy.

Task Force of the European Society of Cardiology the North American Society of Pacing Electrophysiology. (1996). Heart Rate Variability: Standards of Measurement, Physiological Interpretation and Clinical Use. Circulation, 93(5), 1043–1065. https://doi.org/10.1161/01.CIR.93.5.1043.CrossRef

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(2), 81–88. https://doi.org/10.1016/j.neubiorev.2008.08.004.CrossRefPubMed

Toh, G. Y., & Vasey, M. W. (2017). Heterogeneity in autonomic arousal level in perseverative worry: The role of cognitive control and verbal thought. Frontiers in Human Neuroscience, 11, 108. https://doi.org/10.3389/fnhum.2017.00108.CrossRefPubMedPubMedCentral

Vanderlei, L. C. M., Pastre, C. M., Freitas Júnior, I. F., & de Godoy, M. F. (2010). Fractal correlation of heart rate variability in obese children. Autonomic Neuroscience: Basic and Clinical, 155(1–2), 125–129. https://doi.org/10.1016/j.autneu.2010.02.002.CrossRef

Varon, C., Morales, J., Lázaro, J., Orini, M., Deviaene, M., Kontaxis, S., et al. (2020). A comparative study of ECG-derived respiration in ambulatory monitoring using the single-lead ECG. Scientific Reports, 10, 5704. https://doi.org/10.1038/s41598-020-62624-5.

Vasey, M. W., Chriki, L., & Toh, G. Y. (2017). Cognitive control and anxious arousal in worry and generalized anxiety: An initial test of an integrative model. Cognitive Therapy and Research, 41, 155–169. https://doi.org/10.1007/s10608-016-9809-6.CrossRef

Vasey, M. W., El-Hag, N., & Daleiden, E. L. (1996). Anxiety and the processing of emotionally threatening stimuli: Distinctive patterns of selective attention among high- and low-test-anxious children. Child Development, 67(3), 1173–1185. https://doi.org/10.1111/j.1467-8624.1996.tb01789.x.CrossRefPubMed

Vrana, S. R., Cuthbert, B. N., & Lang, P. J. (1986). Fear imagery and text processing. Psychophysiology, 23(3), 247–253. https://doi.org/10.1111/j.1469-8986.1986.tb00626.x.CrossRefPubMed

Widaman, K. F., Helm, J. L., Castro-Schilo, L., Pluess, M., Stallings, M. C., & Belsky, J. (2012). Distinguishing ordinal and disordinal interactions. Psychological Methods, 17(4), 615–622. https://doi.org/10.1037/a0030003.CrossRefPubMedPubMedCentral

Wu, W., & Lang, K. M. (2016). Proportionality assumption in latent basis curve models: A cautionary note. Structural Equation Modeling: A Multidisciplinary Journal, 23(1), 140–154. https://doi.org/10.1080/10705511.2014.938578.CrossRef

Yiend, J., Mathews, A., Burns, T., Dutton, K., Fernández-Martín, A., Georgiou, G. A., et al. (2015). Mechanisms of selective attention in generalized anxiety disorder. Clinical Psychological Science, 3(5), 758–771. https://doi.org/10.1177/2167702614545216.

Zumbo, B. D., Gadermann, A. M., & Zeisser, C. (2007). Ordinal versions of coefficients alpha and theta for Likert rating scales. Journal of Modern Applied Statistical Methods, 6(1), 21–29. https://doi.org/10.22237/jmasm/1177992180.CrossRef

Titel: Inhibitory Control Moderates the Effect of Anxiety on Vagally Mediated Heart Rate Variability: Findings from a Community Sample of Young School-Aged Children
Auteurs: Tonje Grønning Andersen
Charlotte Fiskum
Karl Henry Jacobsen
Stian Lydersen
Lars Wichstrøm
Publicatiedatum: 07-01-2021
Uitgeverij: Springer US
Gepubliceerd in: Cognitive Therapy and Research / Uitgave 4/2021
Print ISSN: 0147-5916
Elektronisch ISSN: 1573-2819
DOI: https://doi.org/10.1007/s10608-020-10184-3

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