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Early institutionalized care disrupts the development of emotion processing in prosody

Published online by Cambridge University Press:  15 February 2021

Lisa K. Chinn ,
Irina Ovchinnikova ,
Anastasia A. Sukmanova ,
Aleksandra O. Davydova  and
Elena L. Grigorenko
Lisa K. Chinn
Affiliation:
Department of Psychology, University of Houston, Houston, TX, USA
Irina Ovchinnikova
Affiliation:
Department of Psychology, University of Houston, Houston, TX, USA
Anastasia A. Sukmanova
Affiliation:
Laboratory of Translational Sciences of Human Development, St Petersburg State University, St Petersburg, Russia
Aleksandra O. Davydova
Affiliation:
Laboratory of Translational Sciences of Human Development, St Petersburg State University, St Petersburg, Russia
Elena L. Grigorenko*
Affiliation:
Department of Psychology, University of Houston, Houston, TX, USA Laboratory of Translational Sciences of Human Development, St Petersburg State University, St Petersburg, Russia Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA Child Study Center and Haskins Laboratories, Yale University, New Haven, CT, USA
*
Author for Correspondence: Elena L. Grigorenko, 4849 Calhoun Rd Rm 373 Health 1 Building/TIMES Houston, Tx 77004; E-mail: elena.grigorenko@times.uh.edu
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Abstract

Millions of children worldwide are raised in institutionalized settings. Unfortunately, institutionalized rearing is often characterized by psychosocial deprivation, leading to difficulties in numerous social, emotional, physical, and cognitive skills. One such skill is the ability to recognize emotional facial expressions. Children with a history of institutional rearing tend to be worse at recognizing emotions in facial expressions than their peers, and this deficit likely affects social interactions. However, emotional information is also conveyed vocally, and neither prosodic information processing nor the cross-modal integration of facial and prosodic emotional expressions have been investigated in these children to date. We recorded electroencephalograms (EEG) while 47 children under institutionalized care (IC) (n = 24) or biological family care (BFC) (n = 23) viewed angry, happy, or neutral facial expressions while listening to pseudowords with angry, happy, or neutral prosody. The results indicate that 20- to 40-month-olds living in IC have event-related potentials (ERPs) over midfrontal brain regions that are less sensitive to incongruent facial and prosodic emotions relative to children under BFC, and that their brain responses to prosody are less lateralized. Children under IC also showed midfrontal ERP differences in processing of angry prosody, indicating that institutionalized rearing may specifically affect the processing of anger.

Keywords

EEGemotion recognitionERPsinstitutionalized careprosody
Type
Special Issue Article
Information
Development and Psychopathology , Volume 33 , Special Issue 2: Honoring the Legacy of Ed Zigler's Lifetime Contributions to Science, Society, and Child Wellbeing , May 2021 , pp. 421 - 430
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press.

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References

Albers, L. H., Johnson, D. E., Hostetter, M. K., Iverson, S., & Miller, L. C. (1997). Health of children adopted from the former Soviet Union and Eastern Europe. Comparison with preadoptive medical records. JAMA, 278, 922–924. doi:10.1001/jama.1997.03550110060037CrossRefGoogle ScholarPubMed
Almas, A. N., Degnan, K. A., Radulescu, A., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2012). Effects of early intervention and the moderating effects of brain activity on institutionalized children's social skills at age 8. Proceedings of the National Academy of Sciences, 109(Supplement 2), 17228–17231. doi:10.1073/pnas.1121256109CrossRefGoogle ScholarPubMed
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models Using lme4. Journal of Statistical Software, 67, 1–48. doi:10.18637/jss.v067.i01CrossRefGoogle Scholar
Batki, A. (2018). The impact of early institutional care on emotion regulation: Studying the play narratives of post-institutionalized and early adopted children. Early Child Development and Care, 188, 1801–1815. doi:10.1080/03004430.2017.1289190CrossRefGoogle Scholar
Batty, M., & Taylor, M. J. (2006). The development of emotional face processing during childhood. Developmental Science, 9, 207–220. doi:10.1111/j.1467-7687.2006.00480.xCrossRefGoogle ScholarPubMed
Castro, V. L., Halberstadt, A. G., Lozada, F. T., & Craig, A. B. (2015). Parents’ emotion-related beliefs, behaviours, and skills predict children's recognition of emotion. Infant and Child Development, 24, 1–22. doi:10.1002/icd.1868CrossRefGoogle ScholarPubMed
Chisholm, K. (1998). A three year follow-up of attachment and indiscriminate friendliness in children adopted from Romanian orphanages. Child Development, 69, 1092–1106. doi:10.2307/1132364CrossRefGoogle ScholarPubMed
Colvert, E., Rutter, M., Beckett, C., Castle, J., Groothues, C., Hawkins, A., … Sonuga-Barke, E. J. S. (2008). Emotional difficulties in early adolescence following severe early deprivation: Findings from the English and Romanian adoptees study. Development and Psychopathology, 20, 547–567. doi:10.1017/S0954579408000278CrossRefGoogle ScholarPubMed
de Haan, M., Nelson, C. A., Gunnar, M. R., & Tout, K. A. (1998). Hemispheric differences in brain activity related to the recognition of emotional expressions by 5-year-old children. Developmental Neuropsychology, 14, 495–518. doi:10.1080/87565649809540725CrossRefGoogle Scholar
Föcker, J., & Röder, B. (2019). Event-related potentials reveal evidence for late integration of emotional prosody and facial expression in dynamic stimuli: An ERP study. Multisensory Research, 32, 473–497. doi:10.1163/22134808-20191332CrossRefGoogle Scholar
Frick, R. W. (1985). Communicating emotion: The role of prosodic features. Psychological Bulletin, 97, 412–429. doi:10.1037/0033-2909.97.3.412CrossRefGoogle Scholar
Fries, A. B. W., & Pollak, S. D. (2004). Emotion understanding in postinstitutionalized Eastern European children. Development and Psychopathology, 16, 355–369. doi:10.1017/s0954579404044554CrossRefGoogle ScholarPubMed
Grossmann, T. (2010). The development of emotion perception in face and voice during infancy. Restorative Neurology and Neuroscience, 28, 219–236. doi:10.3233/RNN-2010-0499CrossRefGoogle ScholarPubMed
Grossmann, T., Striano, T., & Friederici, A. D. (2005). Infants’ electric brain responses to emotional prosody. NeuroReport, 16, 1825–1828. doi:10.1097/01.wnr.0000185964.34336.b1CrossRefGoogle ScholarPubMed
Grossmann, T., Striano, T., & Friederici, A. D. (2006). Crossmodal integration of emotional information from face and voice in the infant brain. Developmental Science, 9, 309–315. doi:10.1111/j.1467-7687.2006.00494.xCrossRefGoogle ScholarPubMed
Halberstadt, A. G., Denham, S. A., & Dunsmore, J. C. (2001). Affective social competence. Social Development, 10, 79–119. doi:10.1111/1467-9507.00150CrossRefGoogle Scholar
Hodges, J., & Tizard, B. (1989). Social and family relationships of ex-institutional adolescents. Journal of Child Psychology and Psychiatry, 30, 77–97. doi:10.1111/j.1469-7610.1989.tb00770.xCrossRefGoogle ScholarPubMed
Hoehl, S., & Wahl, S. (2012). Recording infant ERP data for cognitive research. Developmental Neuropsychology, 37, 187–209. doi:10.1080/87565641.2011.627958CrossRefGoogle ScholarPubMed
Hwa-Froelich, D. A., Matsuo, H., & Becker, J. C. (2014). Emotion identification from facial expressions in children adopted internationally. American Journal of Speech-Language Pathology, 23, 641–654. doi:10.1044/2014_AJSLP-14-0009CrossRefGoogle ScholarPubMed
Kelly, P. A., Viding, E., Wallace, G. L., Schaer, M., De Brito, S. A., Robustelli, B., & McCrory, E. J. (2013). Cortical thickness, surface area, and gyrification abnormalities in children exposed to maltreatment: neural markers of vulnerability? Biological Psychiatry, 74, 845–852. doi:10.1016/j.biopsych.2013.06.020CrossRefGoogle ScholarPubMed
Kendrick, A. (2015). Residential child care. In J. Wright (Ed.), International encyclopedia of the social & behavioral sciences (pp. 534–539). Oxford: Elsevier.10.1016/B978-0-08-097086-8.28077-XCrossRefGoogle Scholar
Kerns, J. G. (2006). Anterior cingulate and prefrontal cortex activity in an FMRI study of trial-to-trial adjustments on the Simon task. NeuroImage, 33, 399–405. doi:10.1016/j.neuroimage.2006.06.012CrossRefGoogle Scholar
Kornilov, S. A., Zhukova, M. A., Ovchinnikova, I. V., Golovanova, I. V., Naumova, O. Y., Logvinenko, T. I., … Grigorenko, E. L. (2019). Language outcomes in adults with a history of institutionalization: Behavioral and neurophysiological characterization. Scientific Reports, 9, 4252. doi:10.1038/s41598-019-40007-9CrossRefGoogle ScholarPubMed
Kungl, M. T., Bovenschen, I., & Spangler, G. (2017). Early adverse caregiving experiences and preschoolers’ current attachment affect brain responses during facial familiarity processing: An ERP study. Frontiers in Psychology, 8, 2047. doi:10.3389/fpsyg.2017.02047CrossRefGoogle Scholar
Lawrence, K., Campbell, R., & Skuse, D. (2015). Age, gender, and puberty influence the development of facial emotion recognition. Frontiers in Psychology, 6, 761. doi:10.3389/fpsyg.2015.00761CrossRefGoogle ScholarPubMed
Leppänen, J. M., & Hietanen, J. K. (2001). Emotion recognition and social adjustment in school-aged girls and boys. Scandinavian Journal of Psychology, 42, 429–435. doi:10.1111/1467-9450.00255CrossRefGoogle ScholarPubMed
Leppänen, J. M., Moulson, M. C., Vogel-Farley, V. K., & Nelson, C. A. (2007). An ERP study of emotional face processing in the adult and infant brain. Child Development, 78, 232–245. doi:10.1111/j.1467-8624.2007.00994.xCrossRefGoogle ScholarPubMed
Marcovitch, S., Goldberg, S., Gold, A., Washington, J., Wasson, C., Krekewich, K., & Handley-Derry, M. (1997). Determinants of behavioural problems in Romanian children adopted in Ontario. International Journal of Behavioral Development, 20, 17–31. doi:10.1080/016502597385414CrossRefGoogle Scholar
Marshall, P. J., Fox, N. A., & Group, B. C. (2004). A comparison of the electroencephalogram between institutionalized and community children in Romania. Journal of Cognitive Neuroscience, 16, 1327–1338. doi:10.1162/0898929042304723CrossRefGoogle ScholarPubMed
Marshall, P. J., Reeb, B. C., Fox, N. A., Nelson, C. A., & Zeanah, C. H. (2008). Effects of early intervention on EEG power and coherence in previously institutionalized children in Romania. Development and Psychopathology, 20, 861–880. doi:10.1017/S0954579408000412CrossRefGoogle ScholarPubMed
McLaughlin, K. A., Sheridan, M. A., Warren, W., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2014). Widespread reductions in cortical thickness following severe early-life deprivation: A neurodevelopmental pathway to ADHD. Biological Psychiatry, 76, 629–638. doi:10.1016/j.biopsych.2013.08.016CrossRefGoogle Scholar
Mehta, M. A., Golembo, N. I., Nosarti, C., Colvert, E., Mota, A., Williams, S. C. R., … Sonuga-Barke, E. J. S. (2009). Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: The English and Romanian adoptees study pilot. Journal of Child Psychology and Psychiatry, 50, 943–951. doi:10.1111/j.1469-7610.2009.02084.xCrossRefGoogle ScholarPubMed
Meyer, M., Alter, K., Friederici, A. D., Lohmann, G., & von Cramon, D. Y. (2002). FMRI reveals brain regions mediating slow prosodic modulations in spoken sentences. Human Brain Mapping, 17, 73–88. doi:10.1002/hbm.10042CrossRefGoogle ScholarPubMed
Moulson, M. C., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2009). Early adverse experiences and the neurobiology of facial emotion processing. Developmental Psychology, 45, 17–30. doi:10.1037/a0014035CrossRefGoogle ScholarPubMed
Muhamedrahimov, R. J., Agarkova, V. V., Vershnina, E. A., Palmov, O. I., Nikiforova, N. V., McCall, R. B., & Groark, C. J. (2014). Behavior problems in children transferred from a socioemotionally depriving institution to St. Petersburg (Russian Federation) families. Infant Mental Health Journal, 35, 111–122. doi:10.1002/imhj.21435CrossRefGoogle Scholar
Mullen, E. M. (1995). Mullen scales of early learning (AGS ed.). Circle Pines, MN: American Guidance Service Inc.Google Scholar
Nelson, C. A., Westerlund, A., McDermott, J. M., Zeanah, C. H., & Fox, N. A. (2013). Emotion recognition following early psychosocial deprivation. Development and Psychopathology, 25, 517–525. doi:10.1017/S0954579412001216CrossRefGoogle ScholarPubMed
Nunez, P. L., & Srinivasan, R. (2006). Electric fields of the brain: The neurophysics of EEG (2nd ed.). New York, NY: Oxford University Press.10.1093/acprof:oso/9780195050387.001.0001CrossRefGoogle Scholar
Nygaard, L. C., & Queen, J. S. (2008). Communicating emotion: Linking affective prosody and word meaning. Journal of Experimental Psychology: Human Perception and Performance, 34, 1017–1030. doi:10.1037/0096-1523.34.4.1017Google ScholarPubMed
Olszanowski, M., Pochwatko, G., Kuklinski, K., Scibor-Rylski, M., Lewinski, P., & Ohme, R. K. (2015). Warsaw set of emotional facial expression pictures: A validation study of facial display photographs. Frontiers in Psychology, 5, 1516. doi: 10.3389/fpsyg.2014.01516CrossRefGoogle ScholarPubMed
Ovchinnikova, I., Zhukova, M. A., Luchina, A., Petrov, M. V., Vasilyeva, M. J., & Grigorenko, E. L. (2019). Auditory mismatch negativity response in institutionalized children. Frontiers in Human Neuroscience, 13, 300. doi:10.3389/fnhum.2019.00300CrossRefGoogle ScholarPubMed
Parker, S. W., Nelson, C. A., & Bucharest Early Intervention Project Core Group. (2005). An event-related potential study of the impact of institutional rearing on face recognition. Development and Psychopathology, 17, 621–639. doi:10.1017/S0954579405050303CrossRefGoogle ScholarPubMed
Petrowski, N., Cappa, C., & Gross, P. (2017). Estimating the number of children in formal alternative care: Challenges and results. Child Abuse & Neglect, 70, 388–398. doi:10.1016/J.CHIABU.2016.11.026CrossRefGoogle ScholarPubMed
Pollak, S. D., Cicchetti, D., Hornung, K., & Reed, A. (2000). Recognizing emotion in faces: Developmental effects of child abuse and neglect. Developmental Psychology, 36, 679–688. doi:10.1037/0012-1649.36.5.679CrossRefGoogle ScholarPubMed
Pollak, S. D., Messner, M., Kistler, D. J., & Cohn, J. F. (2009). Development of perceptual expertise in emotion recognition. Cognition, 110, 242–247. doi:10.1016/J.COGNITION.2008.10.010CrossRefGoogle ScholarPubMed
Pollak, S. D., Nelson, C. A., Schlaak, M. F., Roeber, B. J., Wewerka, S. S., Wiik, K. L., … Gunnar, M. R. (2010). Neurodevelopmental effects of early deprivation in postinstitutionalized children. Child Development, 81, 224–236. doi:10.1111/j.1467-8624.2009.01391.xCrossRefGoogle ScholarPubMed
Roy, P., Rutter, M., & Pickles, A. (2004). Institutional care: Associations between overactivity and lack of selectivity in social relationships. Journal of Child Psychology and Psychiatry, 45, 866–873. doi:10.1111/j.1469-7610.2004.00278.xCrossRefGoogle ScholarPubMed
Tarullo, A. R., & Gunnar, M. R. (2005). Institutional rearing and deficits in social relatedness: Possible mechanisms and processes. Relation to indices of a depressive temperamental style. Cognitie, Creier, Comportament, 9, 329–342.Google Scholar
Tarullo, A. R., Youssef, A., Frenn, K. A., Wiik, K., Garvin, M. C., & Gunnar, M. R. (2016). Emotion understanding, parent mental state language, and behavior problems in internationally adopted children. Development and Psychopathology, 28, 371–383. doi:10.1017/S095457941500111XCrossRefGoogle ScholarPubMed
Töllner, T., Wang, Y., Makeig, S., Müller, H. J., Jung, T.-P., & Gramann, K. (2017). Two independent frontal midline theta oscillations during conflict detection and adaptation in a Simon-type manual reaching task. Journal of Neuroscience, 10, 1752–16. doi:10.1523/JNEUROSCI.1752-16.2017Google Scholar
Tottenham, N., Hare, T. A., Millner, A., Gilhooly, T., Zevin, J. D., & Casey, B. J. (2011). Elevated amygdala response to faces following early deprivation. Developmental Science, 14, 190–204. doi:10.1111/j.1467-7687.2010.00971.xCrossRefGoogle ScholarPubMed
Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., … Casey, B. J. (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Developmental Science, 13, 46–61. doi:10.1111/j.1467-7687.2009.00852.xCrossRefGoogle ScholarPubMed
Vanderwert, R. E., Marshall, P. J., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2010). Timing of intervention affects brain electrical activity in children exposed to severe psychosocial neglect. PloS ONE, 5, e11415. doi:10.1371/journal.pone.0011415CrossRefGoogle ScholarPubMed
Walker-Andrews, A. S. (1986). Intermodal perception of expressive behaviors: Relation of eye and voice? Developmental Psychology, 22, 373–377. doi:10.1037/0012-1649.22.3.373CrossRefGoogle Scholar
Walker-Andrews, A. S., & Lennon, E. (1991). Infants’ discrimination of vocal expressions: Contributions of auditory and visual information. Infant Behavior and Development, 14, 131–142. doi:10.1016/0163-6383(91)90001-9CrossRefGoogle Scholar
West, R., Bailey, K., Tiernan, B. N., Boonsuk, W., & Gilbert, S. (2012). The temporal dynamics of medial and lateral frontal neural activity related to proactive cognitive control. Neuropsychologia, 50, 3450–3460. doi:10.1016/j.neuropsychologia.2012.10.011CrossRefGoogle ScholarPubMed
Whetten, K., Ostermann, J., Whetten, R. A., Pence, B. W., O'Donnell, K., Messer, L. C., … Positive Outcomes for Orphans (POFO) Research Team. (2009). A comparison of the wellbeing of orphans and abandoned children ages 6–12 in institutional and community-based care settings in 5 less wealthy nations. PloS One, 4, e8169. doi:10.1371/journal.pone.0008169CrossRefGoogle ScholarPubMed
Windsor, J., Glaze, L. E., Koga, S. F., & Bucharest Early Intervention Project Core Group. (2007). Language acquisition with limited input: Romanian institution and foster care. Journal of Speech, Language, and Hearing Research, 50, 1365–1381. doi:10.1044/1092-4388(2007/095)CrossRefGoogle ScholarPubMed
Zhu, J., Li, J., Li, X., Rao, J., Hao, Y., Ding, Z., … Wang, G. (2018). Neural basis of the emotional conflict processing in major depression: ERPs and source localization analysis on the N450 and P300 components. Frontiers in Human Neuroscience, 12, article number 214. doi:10.3389/fnhum.2018.00214CrossRefGoogle ScholarPubMed
Zigler, E. F., & Bishop-Josef, S. J. (2006). The cognitive child versus the whole child: Lessons from 40 years of Head Start. In Singer, D. G., Golinkoff, R. M., & Hirsh-Pasek, K. (Eds.), Play = learning: How play motivates and enhances children's cognitive and social-emotional growth (pp. 15–35). Oxford University Press.10.1093/acprof:oso/9780195304381.003.0002CrossRefGoogle Scholar
Zigler, E., & Finn-Stevenson, M. (2007). From research to policy and practice: The school of the 21st century. American Journal of Orthopsychiatry, 77, 175–181. doi:10.1037/0002-9432.77.2.175CrossRefGoogle ScholarPubMed
Zigler, E., & Styfco, S. J. (1997). A “Head Start” in what pursuit? IQ versus social competence as the objective of early intervention. In Devlin, B., Fienberg, S. E., Resnick, D. P., & Roeder, K. (Eds.), Intelligence, genes, and success (pp. 283–314). New York, NY: Springer. doi:10.1007/978-1-4612-0669-9_13CrossRefGoogle Scholar