The objective of the current study was to systematically review the available literature on the relation between behavioral and cardiac indicators used to measure distress in toddlerhood. After ascertaining the eligibility of 2,424 articles through a Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) and PROSPERO (International Prospective Register of Systematic Reviews) guided search process, 22 articles (N = 2,504) that investigated associations between behavioral and cardiac indicators of distress in toddlerhood were identified. The narrative synthesis described the overall relation (direction [positive, negative], strength [Cohen’s D]) between behavioral and cardiac indicators and was organized by cardiac indicator (i.e., heart rate [HR], heart period, respiratory sinus arrhythmia, pre-ejection period) and type of behavior measured (i.e., coding for expressed emotion behaviors vs. emotion regulation behaviors). Methodological characteristics (i.e., timing of measurement for behavioral and cardiac indicators [concurrent, predictive], length of measurement epochs, inclusion of covariates and moderators) were also described. HR was consistently positively (D = .05 to .54) related to expressed emotion behaviors. No other cardiac and behavioral indicators were consistently related. Methodological differences related to behavioral and cardiac indicators utilized, timing of measurement, and length of measurement epochs may be responsible for heterogeneity in findings. The findings suggest that researchers might get divergent results depending on whether distress is measured with cardiac or behavioral indicators of distress in toddlerhood. Suggestions for future psychophysiological research with young children are offered.
AugustineM. E.LeerkesE. M.SmolenA.CalkinsS. D. (2018). Relations between early maternal sensitivity and toddler self-regulation: Exploring variation by oxytocin and dopamine D2 receptor genes. Developmental Psychobiology, 60, 789–804.
2.
BakerE.BaibazarovaE.KtistakiG.SheltonK. H.van GoozenS. H. M. (2012). Development of fear and guilt in young children: Stability over time and relations with psychopathology. Development and Psychopathology, 24, 833–845. https://doi.org/10.1017/S0954579412000399
3.
BarrettL. F. (2013). Psychological construction: The Darwinian approach to the science of emotion. Emotion Review, 5(4), 379–389. https://doi.org/10.1177/1754073913489753
4.
BarrettL. F. (2015). In BarrettL. F.RussellJ. A. (Eds.), The Psychological construction of emotion (pp. 45–79). Guilford.
5.
BarrettL. F.AdolphsR.MarsellaS.MartinezA. M.PollakS. D. (2019). Emotional expressions reconsidered: Challenges to inferring emotion from human facial expressions. Developmental Psychology, 55(9), 1830–1849.
6.
BeauchaineT. 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, 183–214. https://doi.org/10.1017/S0954579401002012
7.
BeauchaineT. P.BellZ.KnaptonE.McConough-CaplanH.ShaderT.ZisnerA. (2019). Respiratory sinus arrhythmia reactivity across empirically-based structural dimensions of psychopathology: A meta-analysis. Psychophysiology, 56, e13329.
8.
BeauchaineT. P.Gatzke-KoppL.MeadH. K. (2007). Polyvagal theory and developmental psychopathology: Emotion dysregulation and conduct problems from preschool to adolescence. Biological Psychology, 74, 174–184. https://doi.org/10.1016/j.biopsycho.2005.08.008
9.
BerntsonG. G.QuigleyK. S.LozanoD. (2007). Cardiovascular psychophysiology. In CacioppoJ. T.TassinaryL. G.BerntsonG. G. (Eds.), Handbook of psychophysiology (pp. 182–210). Cambridge University Press.
10.
BerntsonG. G.UchinoB. N.CacioppoJ. T. (1994). Origins of baseline variance and the law of initial values. Psychophysiology, 31, 204–210.
11.
BocknekE. L.RichardsonP. A.van den HeuvelM. I.QipoT.Brophy-HerbH. E. (2018). Sleep moderates the association between routines and emotion regulation for toddlers in poverty. Journal of Family Psychology, 32(7), 966–974.
BornsteinM. H.SuessP. E. (2000). Child and mother cardiac vagal tone: Continuity, stability, and concordance across the first 5 years. Developmental Psychology, 36(1), 54–65.
15.
BrennerS. L.BeauchaineT. P.SylversP. D. (2005). A Comparison of psychophysiological and self-report measures of behavioral approach and behavioral inhibition. Psychophysiology, 42,108–115.
16.
BrookerR. J.BussK. A. (2010). Dynamic measures of RSA predict distress and regulation in toddlers. Developmental Psychobiology, 52(4), 372–382. https://doi.org/10.1002/dev.20432
17.
BurgessK. B.MarshallP. J.RubinK. H.FoxN. A. (2003). Infant attachment and temperament as predictors of subsequent externalizing problems and cardiac physiology. Journal of Child Psychology and Psychiatry, 44(6), 819–831. https://doi.org/10.1111/1469-7610.00167
18.
BussK. A.GoldsmithH. H. (2007). Biobehavioral approaches to early socioemotional development. In BrownellC. A.KoppC. B (Eds.) Socioemotional development in the toddler years (pp. 370–395). Guilford Press.
19.
BussK. A.GoldsmithH. H.DavidsonR. J. (2005). Cardiac reactivity is associated with changes in negative emotion in 24-month-olds. Developmental Psychobiology. 46, 118–132. https://doi.org/10.1002/dev.20048
20.
CalkinsS. D. (2010). Conceptual and methodological challenges to the study of emotion regulation and psychopathology. Journal of Psychopathology and Behavioral Assessment, 32, 92–95.
21.
CalkinsS. D.DedmonS. E. (2000). Physiological and behavioral regulation in two-year-old children with aggressive/destructive behavior problems. Journal of Abnormal Child Psychology, 28, 103–118.
22.
CalkinsS. D.FoxN. A. (1992). The relations among infant temperament, security of attachment, and behavioral inhibition at twenty-four months. Child Development, 63, 1456–1472. https://doi.org/10.2307/1131568
23.
CalkinsS. D.FoxN. A. (2002). Self-regulatory processes in early personality development: A multilevel approach to the study of childhood social withdrawal and aggression. Development and Psychopathology, 14477–498.
24.
CalkinsS. D.HillA. (2007). Caregiver influences on emerging emotion regulation: Biological and environmental transactions in early development. In GrossJ. J (Ed.), Handbook of emotion regulation (pp. 229–248). The Guilford Press.
25.
CalkinsS. D.JohnsonM. C. (1998). Toddler regulation of distress to frustrating events: Temperamental and maternal correlates. Infant Behavior & Development, 21(3), 379–395. https://doi.org/10.1016/S0163-6383(98)90015-7
26.
CalkinsS. D.LeerkesE. M. (2004). Early attachment processes and the development of emotional self-regulation. In VohsK. D.BaumeisterR. F. (Eds.), Handbook of self-regulation: Research, theory and applications (pp. 324–339). The Guilford Press.
27.
CamposJ. J.CamposR. G.BarrettK. C. (1989). Emergent themes in the study of emotional development and emotion regulation. Developmental Psychology, 25(3), 394–402. https://doi.org/10.1037/0012-1649.25.3.394
28.
CohenJ. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Lawrence Erlbaum Associates.
29.
ColeP. M.HallS. E. (2008). Emotion dysregulation as a risk factor for psychology. In BeauchaineT. P.HinshawS. P. (Eds.), Child and adolescent psychopathology (pp. 265–300). John Wiley and Sons.
30.
ColeP. M.MartinS. E.DennisT. A. (2004). Emotion regulation as a scientific construct: Methodological challenges and directions for child development research. Child Development, 75(2), 317–333. https://doi.org/10.1111/j.1467-8624.2004.00673.x
CrowellS. E.BeauchaineT. P.Gatzke-KoppL.SylversP.MeadH.Chipman-ChaconJ. (2006). Autonomic correlates of attention-deficit/hyperactivity disorder and oppositional defiant disorder in preschool children. Journal of Abnormal Psychology, 115(1), 174–178.
33.
DavidsonR. J.JacksonD. C.KalinN. H. (2000). Emotion, plasticity, context and regulation: Perspectives from affective neuroscience. Psychological Bulletin, 126, 890–906. https://doi.org/10.1037/0033-2909.126.6.890
34.
DomesG.SchulzeL.BöttgerM.GrossmanA.HauensteinK.WirtzP. H.HeinrichsM.HerpertzS. C. (2009). The neural correlates of sex differences in emotional reactivity and regulation. Human Brain Mapping, 31(5), 758–769. https://doi.org/10.1002/hbm.20903
35.
DownsS. H.BlackN. (1998). The Feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. Journal of Epidemiology and Community Health, 52, 377–384. https://doi.org/10.1136/jech.52.6.377
36.
EisenbergN.FabesR. A.MurphyB.MaszkP.SmithM.KarbonM. (1995). The role of emotionality and regulation in children’s social functioning: A longitudinal study. Child Development, 66, 1360–1384. https://www.jstor.org/stable/1131652
37.
EkasN. V.Braungart-RiekerJ. M.MessingerD. S. (2018). The development of infant emotion regulation: Time is of the essence. In ColeP. M.HollesteinT. (Eds.), (pp. 31–51). Emotion regulation: A matter of time.
38.
EnebrinkP.AndershedH.LångströmN. (2005). Callous–unemotional traits are associated with clinical severity in referred boys with conduct problems. Nordic Journal of Psychiatry, 59(6), 431–440. https://doi.org/10.1080/08039480500360690
39.
FowlesD. (1988). Psychophysiology and psychopathology: A motivational approach. Psychophysiology, 25, 373–391.
40.
FoxN. A. (1989). Psychophysiological correlates of emotional reactivity during the first year of life. Developmental Psychology, 25(3), 364–372. https://doi.org/10.1037/0012-1649.25.3.364
41.
FrickP. J.CornellA. H.BarryC. T.BodinS. D.DaneH. E. (2003). Callous-unemotional traits and conduct problems in the prediction of conduct problem severity, aggression, and self-report of delinquency. Journal of Abnormal Child Psychology, 31(4), 457–470. http://resolver.scholarsportal.info/resolve/00910627/v31i0004/457_ctacpisaasod.xml
42.
FunderD. C.OzerD. J. (2019). Evaluating effect size in psychological research: Sense and nonsense. Advances in Methods and Practices in Psychological Science. Advance online publication. https://doi.org/10.1177/2515245919847202
43.
Garcia CollC.KaganJ.ReznickJ. S. (1984). Behavioral inhibition in young children. Child Development, 55(3), 1005–1019. https://www.jstor.org/stable/1130152
44.
Gatzke-KoppL.RamN. (2018). Developmental dynamics of autonomic function in childhood. Psychophysiology, 55, e13218.
45.
GendronM.Feldman BarrettL. (2009). Reconstructing the past: A century of ideas about emotion in psychology. Emotion Review, 1(4), 316–339. https://doi.org/10.1177/1754073909338877
46.
GunnarM. R.VazquezD. (2006). Stress neurobiology and developmental psychopathology. In CicchettiD.CohenD. J. (Eds.), Developmental psychopathology: Developmental neuroscience (pp. 533–577). John Wiley & Sons Inc.
47.
HastingsP. D.NuseloviciJ. N.Klimes-DouganB.KendzioraK. T.UsherB. A.HoM. R.Zahn-WaxlerC. (2009). Dysregulated coherence of subjective and cardiac emotional activation in adolescents with internalizing and externalizing problems. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 50(11), 1348–1356.
48.
HayD. F.van GoozenS. H. M.MundyL.PhillipsR.RobertsS.MeeuwsenM.GoodyerI.PerraO. (2017). If you go down to the woods today: Infants’ distress during a teddy bear’s picnic in relation to peer relations and later emotional problems. Infancy, 22(4), 552–570. https://doi.org/10.1111/infa.12172
49.
HigginsJ. P. T.GreenS. (Eds.). (2011). Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. www.handbook.cochrane.org.
50.
HolzmanJ. B.BridgettD. J. (2017). Heart rate variability indices as bio-markers of top-down self-regulatory mechanisms: A meta-analytic review. Neuroscience & Biobehavioral Review, 74, 233–255.
51.
KaganJ. (1994). Galen’s prophecy: Temperament in human nature. Basic Books.
52.
KaganJ.ReznickJ. S.GibbonsJ. (1989). Inhibited and uninhibited types of children. Child Development, 60(4), 838–845. https://www.jstor.org/stable/1131025
53.
KahleS.MillerJ. G.HelmJ. L.HastingsP. D. (2018). Linking autonomic physiology and emotion regulation in preschoolers: The role of reactivity and recovery. Developmental Psychobiology, 60(7), 775–788.
LabordeS.MosleyE.ThayerJ. F. (2017). Heart rate variability and cardiac vagal tone in psychophysiological research – recommendations for experiment planning, data analysis, and data reporting. Frontiers of Psychology, 8, 213. https://doi.org/10.3389/fpsyg.2017.00213
56.
LiewJ.EisenbergN.SpinradT. L.EggumN. D.HaugenR. G.KupferA.ReiserM. R.SmithC. L.Lemery-ChalfantK.BahamM. E. (2011). Physiological regulation and fearfulness as predictors of young children’s empathy-related reactions. Social Development, 20(1), 111–113. https://doi.org/10.1111/j.1467-9507.2010.00575.x
57.
MatthewsS. G.PhillipsD. I. (2010). Minireview: Transgenerational inheritance of the stress response: A new frontier in stress research. Endocrinology, 151, 7–13. https://doi.org/10.1210/en.2009-0916
58.
MoherD.LiberatiA.TetzlaffJ.AltmanD. G., & The PRISMA Group. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Annals of Internal Medicine, 151, 264–269. https://doi.org/10.7326/0003-4819-151-4-200908180-00135
OberlanderT.SaulJ. P. (2002). Methodological considerations for the use of heart rate variability as a measure of pain reactivity in vulnerable infants. Clinical Perinatology, 29, 427–443. https://doi.org/10.1016/S0095-5108(02)00013-1
61.
ObradovićJ.FinchJ. E. (2017). Linking executive function skills and physiological challenge response: Piecewise growth curve modeling. Developmental Science, 20(6), e12476.
62.
ParetL.BaileyH. N.RocheJ.BureauJ. F.MoranG. (2015) Preschool ambivalent attachment associated with a lack of vagal withdrawal in response to stress. Attachment & Human Development, 17(1), 65–82. https://doi.org/10.1080/14616734.2014.967786
63.
PerryN.CalkinsS. (2018). A biopsychosocial perspective on the development of emotion regulation across childhood. In ColeP. M.HollesteinT. (Eds.), Emotion regulation: A matter of time (pp. 3–30).
64.
PerryN.CalkinsS.BellM. A. (2016) Indirect effects of maternal sensitivity on infant emotion regulation behaviors: The role of vagal withdrawal. Infancy, 21, 128–153.
65.
Pillai RiddellR.RacineN. (2009). Assessing pain in infancy: The caregiver context. Journal of Pain Research and Management, 14(1), 27–32. https://doi.org/10.1155/2009/410725
66.
Pillai RiddellR.FloraD. B.StevensS. A.StevensB.CohenL.GreenbergS.GarfieldH. (2013). Variability in infant acute pain responding meaningfully obscured by averaging pain responses. PAIN, 154, 714–721.
67.
PopayP.RobertsH.SowdenA.PetticrewM.AraiL.RodgersM. (2006). Guidance on the conduct of narrative synthesis in systematic reviews. A product from the ESRC methods programme. Lancaster: Institute of Health Research.
68.
PorgesS. W. (1995). Orienting in a defensive world: Mammalian modifications of our evolutionary heritage: A Polyvagal theory. Psychophysiology, 32, 301–318.
69.
PorgesS. W. (1996). Physiological regulation in high-risk infants: A model for assessment and potential intervention. Development and Psychopathology, 8, 43–58.
70.
PorgesS. W. (2007). The Polyvagal perspective. Biological Psychology74, 116–143.
71.
ProvostM. A.Gouin-DecarieT. (1979). Heart rate reactivity of 9- and 12-months old infants showing specific emotions in natural setting. International Journal of Behavioral Development, 2, 109–120. https://doi.org/10.1177/016502547900200201
72.
QuJ.LeerkesE. M. (2018). Patterns of RSA and observed distress during the still-face paradigm predict later attachment, compliance and behavior problems: A person-centered approach. Developmental Psychobiology60, 707–721.
73.
QuigleyK. S.StifterC. A. (2006). A comparative validation of sympathetic reactivity in children and adults. Psychophysiology43, 357–365.
74.
RothbartM. K.DerryberryD. (1981). Development of individual differences in temperament. In LambM. E.BrownA. L. (Eds.), Advances in developmental psychology (Vol. 1, pp. 39–85). Erlbaum.
75.
RothbartM. K.ZiaieH.BoyleC. G. (1992). Self-regulation and emotion in infancy. In EisenbergN.FabesR. A. (Eds.), Emotion and its regulation in early development (pp. 7–23). San Francisco: Jossey-Bass.
76.
RubinK. H.HastingsP. D.StewartS. L.HendersonH. A.ChenX. (1997). Consistency and concomitants of inhibition: Some of the children, all of the time. Child Development, 68(3), 467–483. https://doi.org/10.1111/j.1467-8624.1997.tb01952.x
77.
SandersonS.TattI. D.HigginsJ. P. (2007). Tools for assessing quality and susceptibility to bias in observational studies in epidemiology: A systematic review and annotated bibliography. International Journal of Epidemiology, 36, 666–676. https://doi.org/10.1093/ije/dym018
78.
SantucciA. K.SilkJ. S.ShawD. S.GentzlerA.FoxN. A.KovacsM. (2008). Vagal tone and temperament as predictors of emotion regulation strategies in young children. Developmental Psychobiology, 50(3), 205–216.
79.
SeiferR.SchillerM.SameroffA. J.ResnickS.RiordanK. (1996). Attachment, maternal sensitivity, and infant temperament during the first year of life. Developmental Psychology, 32(1), 12–25. https://doi.org/10.1037/0012-1649.32.1.12
80.
ShaderT. M.Gatzke-KoppL. M.CrowellS. E.ReidM. J.ThayerJ. F.VaseyM. W.Webster-StrattonC.BellZ.BeauchaineT. P. (2018). Quantifying respiratory sinus arrhythmia: Effects of misspecifying breathing frequencies across development. Development and Psychopathology, 30, 351–366.
81.
SherwoodA.AllenM. T.FahrenbergJ.KelseyR. M.LovalloW. R.van DoorenL. J. P. (1990). Methodological guidelines for impendence cardiography. Psychophysiology, 27, 1–23.
82.
ShirtcliffE. A.VitaccoM. J.GrafA. R.GostishaA. J.MerzJ. L.Zahn-WaxlerC. (2009). Neurobiology of empathy and callousness: Implications for the development of antisocial behavior. Behavioral Sciences & The Law, 27(2), 137–171. https://doi.org/10.1002/bsl.862
83.
SpanglerG.GrossmanK. E. (1993). Biobehavioral organization in securely and insecurely attached infants. Child Development, 64(5), 1439–1450. https://www.jstor.org/stable/1131544
84.
StifterC. A.FoxN. A. (1990). Infant reactivity: Physiological correlates of newborn and 5-month temperament. Developmental Psychology, 26(4), 582. https://doi.org/10.1037/0012-1649.26.4.582
Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. (1996). Heart rate variability: Standards of measurement, physiological interpretation and clinical use. Task force of the European society of cardiology and the North American society of pacing and electrophysiology. Circulation, 93, 1043–1065. https://doi.org/10.1161/01.CIR.93.5.1043
87.
ThompsonR. A. (1994). Emotion regulation: A Theme in search of definition. In FoxN. A. (Ed.), The Development of emotion regulation: Biological and behavioral considerations. Monographs of the Society for Research in Child Development, 59 (Serial No. 240), 25–52.
VoegtlineK. M. (2010). Physiological bases of emotion regulation in young children living in low-income, rural communities. Unpublished doctoral dissertation, The Pennsylvania State University, University Park, Pennsylvania, USA.
90.
von ElmE.AltmanD. G.EggerM.PopcockS. J.GotzscheP. C.VandenbrouckeJ. P. (2007). The Strengthening the reporting of observational studies in epidemiology (STROBE) statement: Guidelines for reporting observational studies. Annals of Internal Medicine, 147(8), 573–577. https://doi.org/10.1371/journal.pmed.0040296
91.
WaxmanJ. A.Pillai RiddellR. R.PinhasovA.SchmidtL. A.TablonP. (2016). Development of cardiovascular indexes of acute pain responding in infants: A systematic review. Pain Research and Management, 16, 1–16. https://doi.org/10.1155/2016/8458696
ZeytinogluS.CalkinsS. D.LeerkesE. M. (2019). Autonomic nervous system functioning in early childhood: Responses to cognitive and negatively valenced emotional challenges. Developmental Psychobiology, 00, 1–17.
94.
Zimmer-GembeckM. J.WebbH. J.PeppingC. A.SwanK.MerloO.SkinnerE. A.AvdagicE.DunbarM. (2017). Review: Is parent-child attachment a correlate of children’s emotion regulation and coping?International Journal of Behavioral Development, 41, 74–93. https://doi.org/10.1177/0165025415618276
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