Hostname: page-component-848d4c4894-ndmmz Total loading time: 0 Render date: 2024-05-21T01:52:07.269Z Has data issue: false hasContentIssue false
  • English
  • Français

The association of temperament and maternal empathy with individual differences in infants’ neural responses to emotional body expressions

Published online by Cambridge University Press:  06 October 2015

Purva Rajhans ,
Manuela Missana ,
Kathleen M. Krol  and
Tobias Grossmann
Purva Rajhans*
Affiliation:
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig
Manuela Missana
Affiliation:
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig
Kathleen M. Krol
Affiliation:
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig
Tobias Grossmann
Affiliation:
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig University of Virginia, Charlottesville
*
Address correspondence and reprint requests to: Purva Rajhans, Early Social Development Group, Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1a, Leipzig 04103, Germany. E-mail: rajhans@cbs.mpg.de.
Get access Rights & Permissions [Opens in a new window]

Abstract

We examined the role of infant temperament and maternal dispositional empathy in the neural processing of happy and fearful emotional body expressions in 8-month-old infants by measuring event-related brain potentials. Our results revealed that infants’ tendency to approach novel objects and people was positively correlated with the neural sensitivity (attention allocation) to fearful expressions, while infant fearfulness was negatively correlated to the neural sensitivity to fearful expressions. Maternal empathic concern was associated with infants’ neural discrimination between happy and fearful expression, with infants of more empathetically concerned mothers showing greater neural sensitivity (attention allocation) to fearful compared to happy expressions. It is critical that our results also revealed that individual differences in the sensitivity to emotional information are explained by an interaction between infant temperament and maternal empathic concern. Specifically, maternal empathy appears to impact infants’ neural responses to emotional body expressions, depending on infant fearfulness. These findings support the notion that the way in which infants respond to emotional signals in the environment is fundamentally linked to their temperament and maternal empathic traits. This adds an early developmental neuroscience dimension to existing accounts of social–emotional functioning, suggesting a complex and integrative picture of why and how infants’ emotional sensitivity varies.

Type
Special Section Articles
Information
Development and Psychopathology , Volume 27 , Issue 4pt1 , November 2015 , pp. 1205 - 1216
Copyright
Copyright © Cambridge University Press 2015 

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.)

References

Ackles, P. K., & Cook, K. G. (1998). Stimulus probability and event-related potentials of the brain in 6-month-old human infants: A parametric study. International Journal of Psychophysiology, 29, 115–143.CrossRefGoogle ScholarPubMed
Atkinson, A. P., Dittrich, W. H., Gemmell, A. J., & Young, A. W. (2004). Emotion perception from dynamic and static body expressions in point-light and full-light displays. Perception, 33, 717–746.CrossRefGoogle ScholarPubMed
Aviezer, H., Trope, Y., & Todorov, A. (2012). Body cues, not facial expressions, discriminate between intense positive and negative emotions. Science, 338, 1225–1229.CrossRefGoogle Scholar
Avinun, R., & Knafo, A. (2013). The Longitudinal Israeli Study of Twins (LIST)—An integrative view of social development. Twin Research and Human Genetics, 1, 1–5.Google Scholar
Bar-Haim, Y., Lamy, D., Pergamin, L., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133, 1–24.CrossRefGoogle ScholarPubMed
Barrett, L. F., Mesquita, B., & Gendron, M. (2011). Context in emotion perception. Current Directions in Psychological Science, 20, 286–290.CrossRefGoogle Scholar
Belsky, J. (2005). Differential susceptibility to rearing influence. In Ellis, B. J. & Bjorklund, D. F. (Eds.), Origins of the social mind: Evolutionary psychology and child development (pp. 139–163). New York: Guilford Press.Google Scholar
Bornemann, B., & Singer, T. (2013). The ReSource training protocol. In Singer, T. & Bolz, M. (Eds.), Compassion: Bridging practice and science (pp. 452–465). Leipzig: Max Planck Institute for Human Cognitive and Brain Sciences.Google Scholar
Brown, C., & Coan, J. A. (in press). The social regulation of neural threat responding. In Freund, L. (Ed.), The social neuroscience of human animal interaction. New York: Taylor & Francis.Google Scholar
Canli, T. (2004). Functional brain mapping of extraversion and neuroticism: Learning from individual differences in emotion processing. Journal of Personality, 72, 1105–1132.CrossRefGoogle ScholarPubMed
Cicchetti, D. (1987). Developmental psychopathology in infancy: Illustration from the study of maltreated youngsters. Journal of Consulting and Clinical Psychology, 55, 837.Google Scholar
Coan, J. A., & Maresh, E. L. (in press). Social baseline theory and the social regulation of emotion. In Gross, J. J. (Ed.), The handbook of emotion regulation (2nd ed.) New York: Guilford Press.Google Scholar
Coan, J. A., Schaefer, H. S., & Davidson, R. J. (2006). Lending a hand social regulation of the neural response to threat. Psychological Science, 17, 1032–1039.CrossRefGoogle Scholar
Davidov, M., Knafo-Noam, A., Serbin, L. A., & Moss, S. (2015). The influential child: How children affect their environment and influence their own risk and resilience. Development and Psychopathology, 27, 947–951 [this issue].CrossRefGoogle ScholarPubMed
Davidson, R. J. (1984). Affect, cognition, and hemispheric specialization. In Izzard, C. E., Kagan, J., & Zajonc, R. (Eds.), Emotions, cognition, and behavior (pp. 320–365). New York: Cambridge University Press.Google Scholar
Davidson, R. J., Kabat-Zinn, J., Schumacher, J., Rosenkranz, M., Muller, D., Santorelli, S. F., et al. (2003). Alterations in brain and immune function produced by mindfulness meditation. Psychosomatic Medicine, 65, 564–570.CrossRefGoogle ScholarPubMed
Davis, M. H. (1980). A multidimensional approach to individual differences in empathy. JSAS Catalog of Selected Documents in Psychology, 10, 85.Google Scholar
Davis, M. H. (1983). Measuring individual differences in empathy: Evidence for a multidimensional approach. Journal of Personality and Social Psychology, 44, 113–136.CrossRefGoogle Scholar
De Gelder, B. (2006). Towards the neurobiology of emotional body language. Nature Reviews Neuroscience, 7, 242–249.CrossRefGoogle ScholarPubMed
Degnan, K. A., & Fox, N. A. (2007). Behavioral inhibition and anxiety disorders: Multiple levels of a resilience process. Development and Psychopathology, 19, 729–746.Google ScholarPubMed
De Haan, M., Belsky, J., Reid, V., Volein, A., & Johnson, M. H. (2004). Maternal personality and infants’ neural and visual responsivity to facial expressions of emotion. Journal of Child Psychology and Psychiatry, 45, 1209–1218.CrossRefGoogle ScholarPubMed
Eisenberg, N., Fabes, R. A., Miller, P. A., Fultz, J., Shell, R., Mathy, R. M., et al. (1989). Relation of sympathy and personal distress to prosocial behavior: A multimethod study. Journal of Personality and Social Psychology, 57, 55–65.Google ScholarPubMed
Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to the environment: An evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 7–28.CrossRefGoogle Scholar
Feshbach, N. D. (1987). Parental empathy and child adjustment-maladjustment. In Eisenberg, N. & Strayer, J. (Eds.), Empathy and its development (pp. 271–291). New York: Cambridge University Press.Google Scholar
Fonagy, P., Gergely, G., & Target, M. (2007). The parent-infant dyad and the construction of the subjective self. Journal of Child Psychology and Psychiatry, 48, 288–328.CrossRefGoogle ScholarPubMed
Fox, N. A. (1991). If it's not left, it's right: Electroencephalograph asymmetry and the development of emotion. American Psychologist, 46, 863.CrossRefGoogle Scholar
Fox, N. A., & Davidson, R. J. (1984). Hemispheric substrates of affect: A developmental model. In Fox, N. A. & Davidson, R. J. (Eds.), The psychobiology of affective development (pp. 353–382). Hillsdale, NJ: Erlbaum.Google Scholar
Frijda, N. H., & Mesquita, B. (1994). The social roles and functions of emotions. In Shinobu, K. & Markus, H. R. (Eds.), Emotion and culture: Empirical studies of mutual influence (pp. 51–87). Washington, DC: American Psychological Association.CrossRefGoogle Scholar
Frith, C. (2009). Role of facial expressions in social interactions. Philosophical Transactions of the Royal Society of London Part B: Biological Sciences, 364, 3453–3458.CrossRefGoogle ScholarPubMed
Gartstein, M. A., & Rothbart, M. K. (2003). Studying infant temperament via the revised infant behavior questionnaire. Infant Behavior and Development, 26, 64–86.CrossRefGoogle Scholar
Goldberg, T. E., & Weinberger, D. R. (2004). Genes and the parsing of cognitive processes. Trends in Cognitive Sciences, 8, 325–335.CrossRefGoogle ScholarPubMed
Gray, J. A. (1982). The neuropsychology of anxiety. New York: Oxford University Press.Google Scholar
Grossmann, T., Johnson, M. H., Vaish, A., Hughes, D. A., Quinque, D., Stoneking, M., et al. (2011). Genetic and neural dissociation of individual responses to emotional expressions in human infants. Developmental Cognitive Neuroscience, 1, 57–66.CrossRefGoogle ScholarPubMed
Kagan, J. (1997). Temperament and the reactions to unfamiliarity. Child Development, 68, 139–143.CrossRefGoogle ScholarPubMed
Kagan, J., & Snidman, N. (2004). The long shadow of temperament. Cambridge, MA: Belknap Press/Harvard University Press.Google Scholar
Kappeler, L., & Meaney, M. J. (2010). Epigenetics and parental effects. Bioessays, 32, 818–827.CrossRefGoogle ScholarPubMed
Kinsbourne, M. E. (1978). Asymmetrical function of the brain. Cambridge: Cambridge University Press.Google Scholar
Klimecki, O. M., Leiberg, S., Lamm, C., & Singer, T. (2013). Functional neural plasticity and associated changes in positive affect after compassion training. Cerebral Cortex, 23, 1552–1561.CrossRefGoogle ScholarPubMed
Klimecki, O. M., Leiberg, S., Ricard, M., & Singer, T. (2013). Differential pattern of functional brain plasticity after compassion and empathy training. Social Cognitive and Affective Neuroscience. Advance online publication.Google Scholar
Knafo, A., & Uzefovsky, F. (2013). Variation in empathy. In Legerstee, M., Haley, W., & Bornstein, M. H. (Eds.), The infant mind: Origins of the social brain (Vol. 97). New York: Guilford Press.Google Scholar
Knafo, A., Zahn-Waxler, C., Davidov, M., Van Hulle, C., Robinson, J. L., & Rhee, S. H. (2009). Empathy in early childhood. Annals of the New York Academy of Sciences, 1167, 103–114.CrossRefGoogle ScholarPubMed
Krol, K. M., Rajhans, P., Missana, M., & Grossmann, T. (2015). Duration of exclusive breastfeeding impacts infant brain responses to emotional body expressions. Frontiers in Behavioral Neuroscience. Advance online publication.CrossRefGoogle Scholar
Lee, I. A., & Preacher, K. J. (2013). Calculation for the test of the diffrenence between two dependent correlations with one variable in common [Computer software]. Retrieved from http://quantpsy.org Google Scholar
Leiberg, S., Klimecki, O., & Singer, T. (2011). Short-term compassion training increases prosocial behavior in a newly developed prosocial game. PLOS ONE, 6, e17798.CrossRefGoogle Scholar
Leppänen, J. M. (2006). Emotional information processing in mood disorders: A review of behavioral and neuroimaging findings. Current Opinion in Psychiatry, 19, 34–39.Google ScholarPubMed
Leppänen, J. M., & Nelson, C. A. (2009). Early development of fear processing. Current Directions in Psychological Science, 21, 200–204.CrossRefGoogle Scholar
Mareschal, D., Johnson, M. H., Sirois, S., Spratling, M., Thomas, M., & Westermann, G. (2007). Neuroconstructivism: Vol. 1. How the brain constructs cognition. Oxford: Oxford University Press.CrossRefGoogle Scholar
Martinos, M., Matheson, A., & de Haan, M. (2012). Links between infant temperament and neurophysiological measures of attention to happy and fearful faces. Journal of Child Psychology and Psychiatry, 53, 1118–1127.CrossRefGoogle ScholarPubMed
Meeren, H. K., van Heijnsbergen, C. C., & De Gelder, B. (2005). Rapid perceptual integration of facial expression and emotional body language. Proceedings of the National Academy of Sciences, 102, 16518–16523.CrossRefGoogle ScholarPubMed
Missana, M., Atkinson, A. P., & Grossmann, T. (2015). Tuning the developing brain to emotional body expressions. Developmental Science, 18, 243–253.CrossRefGoogle Scholar
Missana, M., Rajhans, P., Atkinson, A. P., & Grossmann, T. (2014). The neural processing of happy and fearful body expressions in 8-month old infants. Frontiers in Human Neuroscience, 8, 1–7.CrossRefGoogle Scholar
Nakagawa, A., & Sukigara, M. (2012). Difficulty in disengaging from threat and temperamental negative affectivity in early life: A longitudinal study of infants aged 12–36 months. Behavioral Brain Function, 8, 40.Google ScholarPubMed
Paulus, C. (2009). Der Saarbrücker Persönlichkeitsfragebogen SPF (IRI) zur Messung von Empathie: Psychometrische Evaluation der deutschen Version des Interpersonal Reactivity Index. Unpublished manuscript, Universität des Saarlandes, Saarbrücken.Google Scholar
Peltola, M. J., Leppänen, J. M., Mäki, S., & Hietanen, J. K. (2009). Emer-gence of enhanced attention to fearful faces between 5 and 7 months of age. Social Cognitive and Affective Neuroscience, 4, 134–142.CrossRefGoogle Scholar
Pérez-Edgar, K., Reeb-Sutherland, B. C., McDermott, J. M., White, L. K., Henderson, H. A., Degnan, K., et al. (2011). Attention biases to threat link behavioral inhibition to social withdrawal over time in very young children. Journal of Abnormal Child Psychology, 39, 885–895.CrossRefGoogle ScholarPubMed
Pluess, M., & Belsky, J. (2010). Differential susceptibility to parenting and quality child care. Developmental Psychology, 46, 379.Google ScholarPubMed
Richards, J. E. (2003). Attention affects the recognition of briefly presented visual stimuli in infants: An ERP study. Developmental Science, 6, 312–328.CrossRefGoogle ScholarPubMed
Rosenbaum, J. F., Biederman, J., Bolduc-Murphy, E. A., Faraone, S. V., Chaloff, J., Hirshfeld, D. R., et al. (1993). Behavioral inhibition in childhood: A risk factor for anxiety disorders. Harvard Review of Psychiatry, 1, 2–16.CrossRefGoogle ScholarPubMed
Sharot, T. (2011). The optimism bias. Current Biology, 21, R941–R945.CrossRefGoogle ScholarPubMed
Siegel, D. J. (2007). The mindful brain: Reflection and attunement in the cultivation of well-being (Norton Series on Interpersonal Neurobiology). New York: Norton.Google Scholar
Vaish, A., Grossmann, T., & Woodward, A. (2008). Not all emotions are created equal: The negativity bias in social–emotional development. Psychological Bulletin, 134, 383.CrossRefGoogle ScholarPubMed
Vaughan, H. G., & Kurtzberg, D. (1992). Electrophysiologic indices of human brain maturation and cognitive development. In Gunnar, M. R. & Nelson, C. A. (Eds.), Minnesota symposia on child psychology (pp. 1–36). Hilsdale, NJ: Erlbaum.Google Scholar
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854.CrossRefGoogle ScholarPubMed
Zieber, N., Kangas, A., Hock, A., & Bhatt, R. S. (2013). Infants’ perception of emotion from body movements. Child Development, 85, 675–684.CrossRefGoogle ScholarPubMed
Supplementary material: File

Rajhans supplementary material S1

Supplementary Table

Download Rajhans supplementary material S1(File)
File 12 KB
Supplementary material: File

Rajhans supplementary material S2

Supplementary Table

Download Rajhans supplementary material S2(File)
File 37.2 KB
Supplementary material: File

Rajhans supplementary material S3

Supplementary Figures

Download Rajhans supplementary material S3(File)
File 429 KB
Supplementary material: File

Rajhans supplementary material S4

Supplementary Figures

Download Rajhans supplementary material S4(File)
File 2.1 MB