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Infant autonomic nervous system response and recovery: Associations with maternal risk status and infant emotion regulation

Published online by Cambridge University Press:  17 June 2016

Jill Suurland ,
Kristiaan B. van der Heijden ,
Hanneke J. A. Smaling ,
Stephan C. J. Huijbregts ,
Stephanie H. M. van Goozen  and
Hanna Swaab
Jill Suurland*
Affiliation:
Leiden University
Kristiaan B. van der Heijden
Affiliation:
Leiden University
Hanneke J. A. Smaling
Affiliation:
Leiden University
Stephan C. J. Huijbregts
Affiliation:
Leiden University
Stephanie H. M. van Goozen
Affiliation:
Leiden University Cardiff University
Hanna Swaab
Affiliation:
Leiden University Cardiff University
*
Address correspondence and reprint requests to: Jill Suurland, Department of Clinical Child and Adolescent Studies, Leiden University, Wassenaarseweg 52, Box 9555, 2300 RB Leiden, The Netherlands; E-mail: suurlandj@fsw.leidenuniv.nl.
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Abstract

This study examined whether risk status and cumulative risk were associated with autonomic nervous system reactivity and recovery, and emotion regulation in infants. The sample included 121 6-month-old infants. Classification of risk status was based on World Health Organization criteria (e.g., presence of maternal psychopathology, substance use, and social adversity). Heart rate, parasympathetic respiratory sinus arrhythmia, and sympathetic preejection period were examined at baseline and across the still face paradigm. Infant emotion regulation was coded during the still face paradigm. Infants in the high-risk group showed increased heart rate, parasympathetic withdrawal, and sympathetic activation during recovery from the still face episode. Higher levels of cumulative risk were associated with increased sympathetic nervous system activation. Moreover, increased heart rate during recovery in the high-risk group was mediated by both parasympathetic and sympathetic activity, indicating mobilization of sympathetic resources when confronted with socioemotional challenge. Distinct indirect pathways were observed from maternal risk to infant emotion regulation during the still face paradigm through parasympathetic and sympathetic regulation. These findings underline the importance of specific measures of parasympathetic and sympathetic response and recovery, and indicate that maternal risk is associated with maladaptive regulation of stress early in life reflecting increased risk for later psychopathology.

Type
Regular Articles
Information
Development and Psychopathology , Volume 29 , Issue 3 , August 2017 , pp. 759 - 773
Copyright
Copyright © Cambridge University Press 2016 

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Footnotes

This study is part of MINDS-Leiden (H.S. and S.H.M.v.G., Principal Investigators). The authors thank all families for their participation and the research assistants who contributed to the data collection. This study was funded by Grant 056-23-001 from the National Initiative for Brain and Cognition Research supported and coordinated by the Netherlands Organization for Scientific Research.

References

Alkon, A., Boyce, W. T., Davis, N. V., & Eskenazi, B. (2011). Developmental changes in autonomic nervous system resting and reactivity measures in Latino children from 6 to 60 months of age. Journal of Developmental and Behavioral Pediatrics, 32, 668–677. doi:10.1097/DBP.0b013e3182331fa6 Google Scholar
Alkon, A., Boyce, W. T., Linh, T., Harley, K. G., Neuhaus, J., & Eskenazi, B. (2014). Prenatal adversities and Latino children's autonomic nervous system reactivity trajectories from 6 months to 5 years of age. PLOS ONE, 9. doi:10.1371/journal.pone.0086283 Google Scholar
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, 64–78. doi:10.1002/dev.10082 Google Scholar
Alkon, A., Lippert, S., Vujan, N., Rodriquez, M. E., Boyce, W. T., & Eskenazi, B. (2006). The ontogeny of autonomic measures in 6- and 12-month-old infants. Developmental Psychobiology, 48, 197–208. doi:10.1002/dev.20129 Google Scholar
Bakker, M. J., Tijssen, M. A. J., van der Meer, J. N., Koelman, J. H. T. M., & 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 Scholar
Barker, D. J. P. (1998). In utero programming of chronic disease. Clinical Science, 95, 115–128. doi:10.1042/cs19980019 Google Scholar
Bazhenova, O. V., Plonskaia, O., & Porges, S. W. (2001). Vagal reactivity and affective adjustment in infants during interaction challenges. Child Development, 72, 1314–1326. doi:10.1111/1467-8624.00350 Google Scholar
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, 183–214. doi:10.1017/s0954579401002012 CrossRefGoogle ScholarPubMed
Beauchaine, T., Gatzke-Kopp, L., & Mead, H. K. (2007). Polyvagal theory and developmental psychopathology: Emotion dysregulation and conduct problems from preschool to adolescence. Biological Psychology, 74, 174–184. doi:10.1016/j.biopsycho.2005.08.008 CrossRefGoogle ScholarPubMed
Blair, C., & Peters, R. (2003). Physiological and neurocognitive correlates of adaptive behavior in preschool among children in head start. Developmental Neuropsychology, 24, 479–497. doi:10.1207/s15326942dn2401_04 Google Scholar
Bosquet Enlow, M., King, L., Schreier, H. M. C., Howard, J. M., Rosenfield, D., Ritz, T., et al. (2014). Maternal sensitivity and infant autonomic and endocrine stress responses. Early Human Development, 90, 377–385. doi:10.1016/j.earlhumdev.2014.04.007 Google Scholar
Boyce, W. T., Quas, J., Alkon, A., Smider, N. A., Essex, M. J., Kupfer, D. J., et al. (2001). Autonomic reactivity and psychopathology in middle childhood. British Journal of Psychiatry, 179, 144–150. doi:10.1192/bjp.179.2.144 Google Scholar
Cacioppo, J. T., Uchino, B. N., & Berntson, G. G. (1994). Individual differences in the autonomic origins of heart rate reactivity: The psychometrics of respiratory sinus arrhytmia and preejection period. Psychophysiology, 31, 412–419. doi:10.1111/j.1469-8986.1994.tb02449.x Google Scholar
Calkins, S. D., Dedmon, S. E., Gill, K. L., Lomax, L. E., & Johnson, L. M. (2002). Frustration in infancy: Implications for emotion regulation, physiological processes, and temperament. Infancy, 3, 175–197. doi:10.1207/s15327078in0302_4 Google Scholar
Calkins, S. D., & Keane, S. P. (2004). Cardiac vagal regulation across the preschool period: Stability, continuity, and implications for childhood adjustment. Developmental Psychobiology, 45, 101–112. doi:10.1002/dev.20020 Google Scholar
Campbell, S. B., Shaw, D. S., & Gilliom, M. (2000). Early externalizing behavior problems: Toddlers and preschoolers at risk for later maladjustment. Development and Psychopathology, 12, 467–488. doi:10.1017/s0954579400003114 Google Scholar
Cicchetti, D., & Rogosch, F. A. (1996). Equifinality and multifinality in developmental psychopathology. Development and Psychopathology, 8, 597–600.Google Scholar
Conradt, E., & Ablow, J. (2010). Infant physiological response to the still face paradigm: Contributions of maternal sensitivity and infants’ early regulatory behavior. Infant Behavior & Development, 33, 251–265. doi:10.1016/j.infbeh.2010.01.001 Google Scholar
Degangi, G. A., Dipietro, J. A., Greenspan, S. I., & Porges, S. W. (1991). Psychophysiological characteristics of the regulatory disordered infant. Infant Behavior & Development, 14, 37–50. doi:10.1016/0163-6383(91)90053-u Google Scholar
De Geus, E. J. C., Willemsen, G. H. M., Klaver, C. H. A. M., & Van Doornen, L. J. P. (1995). Ambulatory measurement of respiratory sinus arrhythmia and respiration rate. Biological Psychology, 41, 205–227. doi:10.1016/0301-0511(95)05137-6 Google Scholar
El-Sheikh, M., Arsiwalla, D. D., Hinnant, J. B., & Erath, S. A. (2011). Children's internalizing symptoms: The role of interactions between cortisol and respiratory sinus arrhythmia. Physiology & Behavior, 103, 225–232. doi:10.1016/j.physbeh.2011.02.004 CrossRefGoogle ScholarPubMed
El-Sheikh, M., Erath, S. A., Buckhalt, J. A., Granger, D. A., & Mize, J. (2008). Cortisol and children's adjustment: The moderating role of sympathetic nervous system activity. Journal of Abnormal Child Psychology, 36, 601–611. doi:10.1007/s10802-007-9204-6 CrossRefGoogle ScholarPubMed
Frigerio, A., Ceppi, E., Rusconi, M., Giorda, R., Raggi, M. E., & Fearon, P. (2009). The role played by the interaction between genetic factors and attachment in the stress response in infancy. Journal of Child Psychology and Psychiatry, 50, 1513–1522. doi:10.1111/j.1469-7610.2009.02126.x Google Scholar
Goldsmith, H. H., & Rothbart, M. K. (1999). The Laboratory Temperament Assessment Battery: Description of procedures. Locomotor version. Unpublished manuscript.Google Scholar
Grant, K.-A., McMahon, C., Austin, M.-P., Reilly, N., Leader, L., & Ali, S. (2009). Maternal prenatal anxiety, postnatal caregiving and infants’ cortisol responses to the still face procedure. Developmental Psychobiology, 51, 625–637. doi:10.1002/dev.20397 Google Scholar
Graziano, P., & Derefinko, K. (2013). Cardiac vagal control and children's adaptive functioning: A meta-analysis. Biological Psychology, 94, 22–37. doi:10.1016/j.biopsycho.2013.04.011 Google Scholar
Grossman, P., Van Beek, J., & Wientjes, C. (1990). A comparison of 3 quantification methods for estimations of respiratory sinus arrhythmia Psychophysiology, 27, 702–714. doi:10.1111/j.1469-8986.1990.tb03198.x Google Scholar
Haley, D. W., Handmaker, N. S., & Lowe, J. (2006). Infant stress reactivity and prenatal alcohol exposure. Alcoholism: Clinical and Experimental Research, 30, 2055–2064. doi:10.1111/j.1530-0277.2006.00251.x Google Scholar
Haley, D. W., & Stansbury, K. (2003). Infant stress and parent responsiveness: Regulation of physiology and behavior during still face and reunion. Child Development, 74, 1534–1546. doi:10.1111/1467-8624.00621 Google Scholar
Ham, J., & Tronick, E. (2006). Infant resilience to the stress of the still face: Infant and maternal psychophysiology are related. Annals of the New York Academy of Sciences, 1094, 297–302. doi:10.1196/annals.1376.038 Google Scholar
Hayes, A. F. (2009). Beyond Baron and Kenny: Statistical mediation analysis in the new millennium. Communication Monographs, 76, 408–420. doi:10.1080/03637750903310360 Google Scholar
Hickey, J. E., Suess, P. E., Newlin, D. B., Spurgeon, L., & Porges, S. W. (1995). Vagal tone regulation during sustained attention in boys exposed to opiates in-utero. Addictive Behaviors, 20, 43–59. doi:10.1016/0306-4603(94)00044-y Google Scholar
Hill-Soderlund, A. L., Mills-Koonce, W. R., Propper, C., Calkins, S. D., Granger, D. A., Moore, G. A., et al. (2008). Parasympathetic and sympathetic responses to the strange situation in infants and mothers from avoidant and securely attached dyads. Developmental Psychobiology, 50, 361–376. doi:10.1002/dev.20302 CrossRefGoogle Scholar
Hinnant, J. B., Elmore-Staton, L., & El-Sheikh, M. (2011). Developmental trajectories of respiratory sinus arrhythmia and preejection period in middle childhood. Developmental Psychobiology, 53, 59–68. doi:10.1002/dev.20487 Google Scholar
Hubbard, J. A., Smithmyer, C. M., Ramsden, S. R., Parker, E. H., Flanagan, K. D., Dearing, K. F., et al. (2002). Observational, physiological, and self-report measures of children's anger: Relations to reactive versus proactive aggression. Child Development, 73, 1101–1118. doi:10.1111/1467-8624.00460 Google Scholar
Huijbregts, S. C. J., Seguin, J. R., Zoccolillo, M., Boivin, M., & Tremblay, R. E. (2008). Maternal prenatal smoking, parental antisocial behavior, and early childhood physical aggression. Development and Psychopathology, 20, 437–453. doi:10.1017/s0954579408000217 Google Scholar
Jacob, S., Byrne, M., & Keenan, K. (2009). Neonatal physiological regulation is associated with perinatal factors: A study of neonates born to healthy African American women living in poverty. Infant Mental Health Journal, 30, 82–94. doi:10.1002/imhj.20204 Google Scholar
Kiecolt-Glaser, J. K., & Glaser, R. (1995). Psychoneuroimmunology and health consequences: Data and shared mechanisms. Psychosomatic Medicine, 57, 269–274.Google Scholar
Matthews, K. A., Salomon, K., Kenyon, K., & Allen, M. T. (2002). Stability of children's and adolescents’ hemodynamic responses to psychological challenge: A three-year longitudinal study of a multiethnic cohort of boys and girls. Psychophysiology, 39, 826–834. doi:10.1017/s0048577202011162 CrossRefGoogle ScholarPubMed
McLaughlin, K. A., Sheridan, M. A., Tiby, F., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2015). Causal effects of the early caregiving environment on development of the stress response systems in children. Proceedings of the National Academy of Sciences, 112, 5637–5642. doi:10.1073/pnas.1423363112 Google Scholar
Mejdoubi, J., van den Heijkant, S., Struijf, E., van Leerdam, F., HiraSing, R., & Crijnen, A. (2011). Addressing risk factors for child abuse among high risk pregnant women: Design of a randomised controlled trial of the nurse family partnership in Dutch preventive health care. BMC Public Health, 11, 823–832. doi:10.1186/1471-2458-11-823 Google Scholar
Mesman, J., van IJzendoorn, M. H., & Bakermans-Kranenburg, M. J. (2009). The many faces of the still face paradigm: A review and meta-analysis. Developmental Review, 29, 120–162. doi:10.1016/j.dr.2009.02.001 Google Scholar
Miller, A. L., McDonough, S. C., Rosenblum, K. L., & Sameroff, A. J. (2002). Emotion regulation in context: Situational effects on infant and caregiver behavior. Infancy, 3, 403–433. doi:10.1207/s15327078in0304_01 Google Scholar
Moore, G. A., & Calkins, S. D. (2004). Infants’ vagal regulation in the still face paradigm is related to dyadic coordination of mother-infant interaction. Developmental Psychology, 40, 1068–1080. doi:10.1037/0012-1649.40.6.1068 Google Scholar
Moore, G. A., Hill-Soderlund, A. L., Propper, C. B., Calkins, S. D., Mills-Koonce, W. R., & Cox, M. J. (2009). Mother-infant vagal regulation in the face-to-face still face paradigm is moderated by maternal sensitivity. Child Development, 80, 209–223. doi:10.1111/j.1467-8624.2008.01255.x Google Scholar
Nesse, R. M., & Young, E. A. (2000). Evolutionary origins and functions of the stress response. In Fink, G. (Ed.), Encyclopedia of stress (Vol. 2, pp. 79–84). New York: Academic Press.Google Scholar
Oosterman, M., de Schipper, J. C., Fisher, P., Dozier, M., & Schuengel, C. (2010). Autonomic reactivity in relation to attachment and early adversity among foster children. Development and Psychopathology, 22, 109–118. doi:10.1017/s0954579409990290 Google Scholar
Porges, S. W. (2003). The polyvagal theory: Phylogenetic contributions to social behavior. Physiology & Behavior, 79, 503–513. doi:10.1016/s0031-9384(03)00156-2 Google Scholar
Porges, S. W. (2007). A phylogenetic journey through the vague and ambiguous Xth cranial nerve: A commentary on contemporary heart rate variability research. Biological Psychology, 74, 301–307. doi:10.1016/j.biopsycho.2006.08.007 Google Scholar
Porges, S. W., & Furman, S. A. (2011). The early development of the autonomic nervous system provides a neural platform for social behaviour: A polyvagal perspective. Infant and Child Development, 20, 106–118. doi:10.1002/icd.688 Google Scholar
Preacher, K. J., & Hayes, A. F. (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods, 40, 879–891. doi:10.3758/BRM.40.3.879 Google Scholar
Propper, C., & Holochwost, S. J. (2013). The influence of proximal risk on the early development of the autonomic nervous system. Developmental Review, 33, 151–167. doi:10.1016/j.dr.2013.05.001 Google Scholar
Quigley, K. S., & Stifter, C. A. (2006). A comparative validation of sympathetic reactivity in children and adults. Psychophysiology, 43, 357–365. doi:10.1111/j.1469-8986.2006.00405.x CrossRefGoogle ScholarPubMed
Randall, W. C., Randall, D. C., & Ardell, J. L. (1991). Autonomic regulation of myocardial contractility. In Zuckerman, I. H. & Gilmore, J. P. (Eds.), Reflex control of circulation (pp. 39–65). Boca Raton, FL: CRC Press.Google Scholar
Reijman, S., Alink, L. R. A., Compier-de Bock, L. H. C. G., Werner, C. D., Maras, A., Rijnberk, C., et al. (2014). Autonomic reactivity to infant crying in maltreating mothers. Child Maltreatment, 19, 101–112. doi:10.1177/1077559514538115 Google Scholar
Repetti, R. L., Taylor, S. E., & Seeman, T. E. (2002). Risky families: Family social environments and the mental and physical health of offspring. Psychological Bulletin, 128, 330–366. doi:10.1037//0033-2909.128.2.330 Google Scholar
Riese, H., Groot, P. F. C., Van den Berg, M., Kupper, N. H. M., Magnee, E. H. B., Rohaan, E. J., et al. (2003). Large-scale ensemble averaging of ambulatory impedance cardiograms. Behavior Research Methods, Instruments,and Computers, 35, 467–477. doi:10.3758/bf03195525 Google Scholar
Schuetze, P., Eiden, R. D., Colder, C. R., Gray, T. R., & Huestis, M. A. (2013). Physiological regulation at 9 months of age infants prenatally exposed to cigarettes. Infancy, 18, 233–255. doi:10.1111/j.1532-7078.2012.00118.x Google Scholar
Smaling, H. J., Huijbregts, S. C., Suurland, J., Van der Heijden, K. B., Van Goozen, S. H. M., & Swaab, H. (2015). Prenatal reflective functioning in primiparous women with a high-risk profile. Infant Mental Health Journal, 36, 251–261. doi:10.1002/imhj.21506 CrossRefGoogle ScholarPubMed
Stifter, C. A., & Spinrad, T. L. (2002). The effect of excessive crying on the development of emotion regulation. Infancy, 3, 133–152. doi:10.1207/s15327078in0302_2 CrossRefGoogle ScholarPubMed
Tronick, E., Als, H., Adamson, L., Wise, S., & Brazelton, T. B. (1978). Infants response to entrapment between contradictory messages in face-to-face interaction. Journal of the American Academy of Child & Adolescent Psychiatry, 17, 1–13. doi:10.1016/s0002-7138(09)62273-1 Google Scholar
Van Dijk, A. E., Van Eijsden, M., Stronks, K., Gemke, R. J. B. J., & Vrijkotte, T. G. M. (2012). Prenatal stress and balance of the child's cardiac autonomic nervous system at age 5–6 years. PLOS ONE, 7. doi:10.1371/journal.pone.0030413 Google Scholar
Van Vliet, I. M., Leroy, H., & Van Megen, H. J. G. M. (2000). MINI plus. International Neuropsychological Interview. Nederlandse Versie 5.0.0 [Dutch Version 5.0.0.]. Unpublished manuscript.Google Scholar
Weinberg, M. K., & Tronick, E. Z. (1996). Infant affective reactions to the resumption of maternal interaction after the still face. Child Development, 67, 905–914. doi:10.1111/j.1467-8624.1996.tb01772.x Google Scholar
Weinberg, M. K., Tronick, E. Z., & Cohn, J. F. (1999). Gender differences in emotional expressivity and self-regulation during early infancy. Developmental Psychology, 35, 175–188. doi:10.1037/0012-1649.35.1.175 Google Scholar
Willemsen, G. H. M., De Geus, E. J. C., Klaver, C. H. A. M., Van Doornen, L. J. P., & Carroll, D. (1996). Ambulatory monitoring of the impedance cardiogram. Psychophysiology, 33, 184–193. doi:10.1111/j.1469-8986.1996.tb02122.x Google Scholar
World Health Organization. (2005). Child abuse and neglect. Retrieved from http://who.int/violence_injury_prevention/violence/neglect/en/print.html Google Scholar
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