Skip to main content Accessibility help
Hostname: page-component-684899dbb8-vtfg7 Total loading time: 0.306 Render date: 2022-05-24T18:13:20.138Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true }

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*
Leiden University
Kristiaan B. van der Heijden
Leiden University
Hanneke J. A. Smaling
Leiden University
Stephan C. J. Huijbregts
Leiden University
Stephanie H. M. van Goozen
Leiden University Cardiff University
Hanna Swaab
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:


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.

Regular Articles
Copyright © Cambridge University Press 2016 

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.)


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.


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, 668677. doi:10.1097/DBP.0b013e3182331fa6 CrossRefGoogle 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 CrossRefGoogle 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, 6478. doi:10.1002/dev.10082 CrossRefGoogle 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, 197208. doi:10.1002/dev.20129 CrossRefGoogle 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, 314322.Google Scholar
Barker, D. J. P. (1998). In utero programming of chronic disease. Clinical Science, 95, 115128. doi:10.1042/cs19980019 CrossRefGoogle ScholarPubMed
Bazhenova, O. V., Plonskaia, O., & Porges, S. W. (2001). Vagal reactivity and affective adjustment in infants during interaction challenges. Child Development, 72, 13141326. doi:10.1111/1467-8624.00350 CrossRefGoogle ScholarPubMed
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, 183214. 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, 174184. doi:10.1016/j.biopsycho.2005.08.008 CrossRefGoogle Scholar
Blair, C., & Peters, R. (2003). Physiological and neurocognitive correlates of adaptive behavior in preschool among children in head start. Developmental Neuropsychology, 24, 479497. doi:10.1207/s15326942dn2401_04 CrossRefGoogle ScholarPubMed
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, 377385. doi:10.1016/j.earlhumdev.2014.04.007 CrossRefGoogle ScholarPubMed
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, 144150. doi:10.1192/bjp.179.2.144 CrossRefGoogle ScholarPubMed
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, 412419. doi:10.1111/j.1469-8986.1994.tb02449.x CrossRefGoogle 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, 175197. doi:10.1207/s15327078in0302_4 CrossRefGoogle 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, 101112. doi:10.1002/dev.20020 CrossRefGoogle ScholarPubMed
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, 467488. doi:10.1017/s0954579400003114 CrossRefGoogle ScholarPubMed
Cicchetti, D., & Rogosch, F. A. (1996). Equifinality and multifinality in developmental psychopathology. Development and Psychopathology, 8, 597600.CrossRefGoogle 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, 251265. doi:10.1016/j.infbeh.2010.01.001 CrossRefGoogle ScholarPubMed
Degangi, G. A., Dipietro, J. A., Greenspan, S. I., & Porges, S. W. (1991). Psychophysiological characteristics of the regulatory disordered infant. Infant Behavior & Development, 14, 3750. doi:10.1016/0163-6383(91)90053-u CrossRefGoogle 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, 205227. doi:10.1016/0301-0511(95)05137-6 CrossRefGoogle ScholarPubMed
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, 225232. 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, 601611. 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, 15131522. doi:10.1111/j.1469-7610.2009.02126.x CrossRefGoogle 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, 625637. doi:10.1002/dev.20397 CrossRefGoogle ScholarPubMed
Graziano, P., & Derefinko, K. (2013). Cardiac vagal control and children's adaptive functioning: A meta-analysis. Biological Psychology, 94, 2237. doi:10.1016/j.biopsycho.2013.04.011 CrossRefGoogle Scholar
Grossman, P., Van Beek, J., & Wientjes, C. (1990). A comparison of 3 quantification methods for estimations of respiratory sinus arrhythmia Psychophysiology, 27, 702714. doi:10.1111/j.1469-8986.1990.tb03198.x CrossRefGoogle Scholar
Haley, D. W., Handmaker, N. S., & Lowe, J. (2006). Infant stress reactivity and prenatal alcohol exposure. Alcoholism: Clinical and Experimental Research, 30, 20552064. doi:10.1111/j.1530-0277.2006.00251.x CrossRefGoogle ScholarPubMed
Haley, D. W., & Stansbury, K. (2003). Infant stress and parent responsiveness: Regulation of physiology and behavior during still face and reunion. Child Development, 74, 15341546. doi:10.1111/1467-8624.00621 CrossRefGoogle 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, 297302. doi:10.1196/annals.1376.038 CrossRefGoogle ScholarPubMed
Hayes, A. F. (2009). Beyond Baron and Kenny: Statistical mediation analysis in the new millennium. Communication Monographs, 76, 408420. doi:10.1080/03637750903310360 CrossRefGoogle 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, 4359. doi:10.1016/0306-4603(94)00044-y CrossRefGoogle ScholarPubMed
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, 361376. 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, 5968. doi:10.1002/dev.20487 CrossRefGoogle ScholarPubMed
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, 11011118. doi:10.1111/1467-8624.00460 CrossRefGoogle ScholarPubMed
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, 437453. doi:10.1017/s0954579408000217 CrossRefGoogle ScholarPubMed
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, 8294. doi:10.1002/imhj.20204 CrossRefGoogle ScholarPubMed
Kiecolt-Glaser, J. K., & Glaser, R. (1995). Psychoneuroimmunology and health consequences: Data and shared mechanisms. Psychosomatic Medicine, 57, 269274.CrossRefGoogle ScholarPubMed
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, 826834. 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, 56375642. doi:10.1073/pnas.1423363112 CrossRefGoogle ScholarPubMed
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, 823832. doi:10.1186/1471-2458-11-823 CrossRefGoogle ScholarPubMed
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, 120162. doi:10.1016/j.dr.2009.02.001 CrossRefGoogle 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, 403433. doi:10.1207/s15327078in0304_01 CrossRefGoogle 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, 10681080. doi:10.1037/0012-1649.40.6.1068 CrossRefGoogle ScholarPubMed
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, 209223. doi:10.1111/j.1467-8624.2008.01255.x CrossRefGoogle ScholarPubMed
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. 7984). 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, 109118. doi:10.1017/s0954579409990290 CrossRefGoogle ScholarPubMed
Porges, S. W. (2003). The polyvagal theory: Phylogenetic contributions to social behavior. Physiology & Behavior, 79, 503513. doi:10.1016/s0031-9384(03)00156-2 CrossRefGoogle 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, 301307. doi:10.1016/j.biopsycho.2006.08.007 CrossRefGoogle ScholarPubMed
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, 106118. doi:10.1002/icd.688 CrossRefGoogle ScholarPubMed
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, 879891. doi:10.3758/BRM.40.3.879 CrossRefGoogle Scholar
Propper, C., & Holochwost, S. J. (2013). The influence of proximal risk on the early development of the autonomic nervous system. Developmental Review, 33, 151167. doi:10.1016/j.dr.2013.05.001 CrossRefGoogle Scholar
Quigley, K. S., & Stifter, C. A. (2006). A comparative validation of sympathetic reactivity in children and adults. Psychophysiology, 43, 357365. 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. 3965). 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, 101112. doi:10.1177/1077559514538115 CrossRefGoogle ScholarPubMed
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, 330366. doi:10.1037//0033-2909.128.2.330 CrossRefGoogle ScholarPubMed
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, 467477. doi:10.3758/bf03195525 CrossRefGoogle ScholarPubMed
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, 233255. doi:10.1111/j.1532-7078.2012.00118.x CrossRefGoogle ScholarPubMed
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, 251261. 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, 133152. doi:10.1207/s15327078in0302_2 CrossRefGoogle Scholar
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, 113. doi:10.1016/s0002-7138(09)62273-1 CrossRefGoogle ScholarPubMed
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 CrossRefGoogle ScholarPubMed
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, 905914. doi:10.1111/j.1467-8624.1996.tb01772.x CrossRefGoogle 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, 175188. doi:10.1037/0012-1649.35.1.175 CrossRefGoogle ScholarPubMed
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, 184193. doi:10.1111/j.1469-8986.1996.tb02122.x CrossRefGoogle ScholarPubMed
World Health Organization. (2005). Child abuse and neglect. Retrieved from Google Scholar
Supplementary material: File

Suurland supplementary material

Tables S1-S3

Download Suurland supplementary material(File)
File 43 KB
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the or variations. ‘’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

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

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

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

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

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

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *