I.P. Pavlov Journal of Higher Nervous ActivityI.P. Pavlov Journal of Higher Nervous ActivityЖурнал высшей нервной деятельности им. И.П. Павлова0044-46773034-5316The Russian Academy of Sciences65204210.31857/S0044467723020089GITMPKОБЗОРЫ И ТЕОРЕТИЧЕСКИЕ СТАТЬИFORMATION OF PROSOCIAL BEHAVIOR AND ITS NEUROPHYSIOLOGICAL MECHANISMS IN EARLY CHILDHOODСтановление просоциального поведения в раннем детстве и его нейрофизиологические механизмыPavlenkoV. B.ПавленкоВ. Б.vpav55@gmail.comOrekhovaL. S.ОреховаЛ. С.vpav55@gmail.comPortugalskayaA. A.ПортугальскаяА. А.vpav55@gmail.comMikhailovaA. A.МихайловаА. А.vpav55@gmail.comV.I. Vernadsky Crimean Federal UniversityКрымский федеральный университет им. В.И. Вернадского0103202373219321302022025Copyright ©; 2023, В.Б. Павленко, Л.С. Орехова, А.А. Португальская, А.А. МихайловаCopyright ©; 2023, В.Б. Павленко, Л.С. Орехова, А.А. Португальская, А.А. Михайлова2023В.Б. Павленко, Л.С. Орехова, А.А. Португальская, А.А. МихайловаВ.Б. Павленко, Л.С. Орехова, А.А. Португальская, А.А. Михайловаhttps://innoscience.ru/0044-4677/article/view/652042

From a very early age children are capable on prosocial acts: giving objects, comforting and sharing with other people. This review considers modern research on the patterns and neurophysiological mechanisms of helping behavior (HB) formation in early childhood, including the results of the authors’ own work. Methods for HB researching in infants and young children are presented. The factors of development and neurophysiological mechanisms of instrumental, empathic and altruistic HB, and the role of empathy in these kinds of behaviors are analyzed. We also described data about involvement of various brain structures (for example, the mirror system as extended part of sensorimotor and emotional neural networks) in implementation of HB. The importance of research into the mechanisms of prosocial behavior for the full-fledged upbringing and education of children in the conditions of modern society is emphasized.

Дети с самого раннего возраста способны на просоциальные поступки: подают предметы, утешают и делятся с другими людьми. В данном обзоре рассматриваются современные исследования закономерностей и нейрофизиологических механизмов становления помогающего поведения (ПП) в раннем детстве, в том числе результаты собственных работ авторов. Представлены методы изучения ПП у детей младенческого и раннего возраста. Анализируются факторы развития и нейрофизиологические механизмы инструментального, эмпатического и альтруистического ПП, роль эмпатии в его запуске. Приводятся данные об участии в реализации ПП различных мозговых структур, а также зеркальной системы мозга, расширенная часть которой включает сенсомоторную и эмоциональную нейронные сети. Подчеркивается значение исследований механизмов просоциального поведения для полноценного воспитания и обучения детей в условиях современного общества.

childrenprosocial behaviorhelping behaviorEEG mu-rhythmmirror neuronsдетипросоциальное поведениепомогающее поведениемю-ритм ЭЭГзеркальные нейроныАрутюнова К.Р., Созинова И.М., Александров Ю.И. Мозговые основы моральной оценки действий. Современная зарубежная психология. 2020. 9 (2): 68–81.Базян А.С. Зеркальные нейроны, физиологическая роль, особенности функционирования и эмоционально насыщенная когнитивная карта мозга. Успехи физиол. наук. 2019. 50 (2): 42–62.Бушов Ю.В., Ушаков В.Л., Светлик М.В., Карташов С.И., Орлов В.А. Роль зеркальных нейронов в интерпретации действий и намерений. Вестник Томского государственного университета. Биология. 2021. 56: 86–107.Знаменская И.И., Созинова И.М., Александров Ю.И. Интуитивные и рациональные компоненты морального выбора у детей 3–11 лет. Теоретическая и экспериментальная психология. 2013. 6 (2): 57–70.Курганский А.В. Оценка управляющих функций у детей 3-6 лет: состояние, проблемы и перспективы. Журн. высш. нервн. деят. им. И.П. Павлова. 2021. 71 (4): 468–484.Ларионова Е.В. Гарах Ж.В., Зайцева Ю.С. Мю-ритм в современных исследованиях: теоретические и методологические аспекты. Журн. высш. нервн. деят. им. И.П. Павлова. 2022. 72 (1): 11–35.Лебедева Н.Н., Зуфман А.И., Мальцев В.Ю. Система зеркальных нейронов мозга: ключ к обучению, формированию личности и пониманию чужого сознания. Успехи физиологических наук. 2017. 48 (4): 16–28.Лебедева Н.Н., Каримова Е.Д., Карпычев В.В., Мальцев В.Ю. Зеркальная система мозга при наблюдении, выполнении и представлении моторных задач – нейрофизиологическое отражение восприятия чужого сознания. Журн. высш. нервн. деят. им. И.П. Павлова. 2018. 2: 204–215.Лебедева Н.Н., Буркитбаев С.Е., Каримова Е.Д. Активация зеркальной системы мозга зависит от способа предъявления стимулов: непосредственно экспериментатором или как видеоролик. Журн. высш. нервн. деят. им. И.П. Павлова. 2020. 70 (4): 460–472.Михайлова А.А., Орехова Л.С., Махин С.А., Павленко В.Б. Реактивность сенсомоторных ритмов ЭЭГ при наблюдении за про- и антисоциальными действиями у детей в раннем возрасте. Журн. высш. нервн. деят. им. И.П. Павлова. 2022. 72 (2): 217–226.Михайлова А.А., Орехова Л.С., Дягилева Ю.О., Мухтаримова Т.И., Павленко В.Б. Реактивность мю-ритма ЭЭГ при наблюдении и выполнении действий у детей раннего возраста, имеющих разный уровень развития рецептивной речи. Журн. высш. нервн. деят. им. И.П. Павлова. 2020. 70 (3): 422–432.Cимонов П.В. Мотивированный мозг. М.: Наука, 1987. 269 с.Юдина Т.О., Котова Т.Н. Развитие просоциального поведения у детей раннего возраста. Шаги/Steps. 2015. 1 (1): 108–121.Юдина Т.О. Эмпатия и мораль: место встречи (обзор зарубежных исследований). Шаги/Steps. 2017. 3 (1): 28–39.Addabbo M., Bolognini N., Turati C. Neural time course of pain observation in infancy. Dev Sci. 2021. 24 (4): 13074.Arnett K., Roach A., Elzy M., Jelsone-Swain L. Childhood emotional invalidation and right hemispheric mu suppression during a pain empathy task: An EEG study. Soc Neurosci. 2019. 14 (2): 236–250.Bastiaansen J.A., Thioux M., Keysers C. Evidence for mirror systems in emotions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009. 364 (1528): 2391–2404.Bekkali S., Youssef G.J., Donaldson P.H., Albein-Urios N., Hyde C., Enticott P.G. Is the putative mirror neuron system associated with empathy? A systematic review and meta-analysis. Neuropsychol Rev. 2021. 31 (1): 14–57.Berboth S., Morawetz C. Amygdala-prefrontal connectivity during emotion regulation: A meta-analysis of psychophysiological interactions. Neuropsychologia. 2021. 153: 107767.Bimbi M., Festante F., Coudé G., Vanderwert R.E., Fox N.A., Ferrari P.F. Simultaneous scalp recorded EEG and local field potentials from monkey ventral premotor cortex during action observation and execution reveals the contribution of mirror and motor neurons to the mu-rhythm. Neuroimage. 2018. 175: 22–31.Bonini L., Rotunno C., Arcuri E., Gallese V. Mirror neurons 30 years later: implications and applications. Trends Cogn Sci. 2022. 26 (9): 767–781.Bowman L.C., Thorpe S.G., Cannon E.N., Fox N.A. Action mechanisms for social cognition: behavioral and neural correlates of developing Theory of Mind. Dev Sci. 2017. 20 (5).https://doi.org/10.1111/desc.12447Brownell C.A., Svetlova M., Anderson R., Nichols S., Drummond J. Socialization of early prosocial behavior: parents’ talk about emotions is associated with sharing and helping in toddlers. Infancy. 2013. 18 (1): 91–119.Cowell J.M., Decety J. Precursors to morality in development as a complex interplay between neural, socio-environmental, and behavioral facets. Proc. Natl. Acad. Sci. USA. 2015. 112: 12657–12662.Craighero L., Mele S. Equal kinematics and visual context but different purposes: Observer’s moral rules modulate motor resonance. Cortex. 2018. 104: 1–11.Dahl A., Killen M. A Developmental perspective on the origins of morality in infancy and early childhood. Front Psychol. 2018. 9: 1736.Dahl A., Brownell C.A. The social origins of human prosociality. Curr Dir Psychol Sci. 2019. 28 (3): 274–279.Dahl A., Goeltz M.T., Brownell C.A. Scaffolding the emergence of infant helping: A longitudinal experiment. Child Dev. 2022. 93 (3): 751–759.Datko M., Pineda J.A., Müller R.A. Positive effects of neurofeedback on autism symptoms correlate with brain activation during imitation and observation. Eur. J. Neurosci. 2018. 47 (6): 579–591.De Freitas J., Thomas K., DeScioli P., Pinker S. Common knowledge, coordination, and strategic mentalizing in human social life. PNAS. 2019. 116 (28): 13751–13758.De Renzi E., Cavalleri F., Facchini S. Imitation and utilisation behavior. J. Neurol. Neurosurg. Psychiatry. 1996. 61 (4): 396–400.Debnath R., Salo V.C., Buzzell G.A., Yoo K.H., Fox N.A. Mu rhythm desynchronization is specific to action execution and observation: Evidence from time-frequency and connectivity analysis. Neuroimage. 2019. 184: 496–507.Decety J., Svetlova M. Putting together phylogenetic and ontogenetic perspectives on empathy. Dev Cogn Neurosci. 2012. 2 (1): 1–24.Decety J., Bartal I.B., Uzefovsky F., Knafo-Noam A. Empathy as a driver of prosocial behaviour: highly conserved neurobehavioural mechanisms across species. Philos Trans R Soc Lond B Biol Sci. 2016. 371 (1686): 20150077.Decety J., Meidenbauer K.L., Cowell J.M. The development of cognitive empathy and concern in preschool children: A behavioral neuroscience investigation. Dev Sci. 2018. 21 (3): e12570.Decety J., Holvoet C. The emergence of empathy: A developmental neuroscience perspective. Dev Rev. 2021. 62: 100999.di Pellegrino G., Fadiga L., Fogassi L., Gallese V., Rizzolatti G. Understanding motor events: a neurophysiological study. Exp. Brain Res. 1992. 91 (1): 176–180.Drummond J., Paul E.F., Waugh W.E., Hammond S.I., Brownell C.A. Here, there and everywhere: emotion and mental state talk in different social contexts predicts empathic helping in toddlers. Front Psychol. 2014. 5: 361.Dunfield K., Kuhlmeier V.A., O’Connell L., Kelley E. Examining the Diversity of Prosocial Behavior: Helping, Sharing, and Comforting in Infancy. Infancy. 2011. 16 (3): 227–247.Dunfield K., Kuhlmeier V.A. Classifying prosocial behavior: Children’s responses to instrumental need, emotional distress, and material desire. Child Development. 2013. 84 (5): 1766–1776.Dunfield K.A. A construct divided: prosocial behavior as helping, sharing, and comforting subtypes. Front Psychol. 2014. 5: 958.Dunfield K.A., Best L.J., Kelley E.A., Kuhlmeier V.A. Motivating moral behavior: helping, sharing, and comforting in young children with Autism Spectrum Disorder. Front Psychol. 2019. 10: 25.Eisenberg N., Fabes R.A., Spinrad T. Prosocial development. In Handbookof Child Psychology. Ed. Eisenberg N. N.Y.: Wiley, 2006. 646–718 p.Filippi C.A., Cannon E.N., Fox N.A., Thorpe S G., Ferrari P.F., Woodward A.L. Motor system activation predicts goal imitation in 7-month-old infants. Psychol Sci. 2016. 27 (5): 675–684.Fox N.A., Bakermans-Kranenburg M.J., Yoo K.H., Bowman L.C., Cannon E.N., Vanderwert R.E., Ferrari P.F., van IJzendoorn M.H. Assessing human mirror activity with EEG mu rhythm: A meta-analysis. Psychol Bull. 2016. 142 (3): 291–313.Friedrich E.V., Sivanathan A., Lim T., Suttie N., Louchart S., Pillen S., Pineda J.A. An effective neurofeedback intervention to improve social interactions in children with Autism Spectrum Disorder. J. Autism. Dev. Disord. 2015. 45 (12): 4084–4100.Genzer S., Ong D.C., Zaki J., Perry A. Mu rhythm suppression over sensorimotor regions is associated with greater empathic accuracy. Soc. Cogn. Affect Neurosci. 2022. 17 (9): 788–801.Giner Torréns M., Dreizler K., Kärtner J. Insight into toddlers’ motivation to help: From social participants to prosocial contributors. Infant Behav Dev. 2021. 64: 101603.Gredebäck G., Kaduk K., Bakker M., Gottwald J., Ekberg T., Elsner C., Reid V., Kenward B. The neuropsychology of infants’ pro-social preferences. Dev. Cogn. Neurosci. 2015. 12: 106–113.Green A., Siposova B., Kita S., Michael J. Stopping at nothing: Two-year-olds differentiate between interrupted and abandoned goals. J. Exp. Child. Psychol. 2021. 209: 105171.Grueneisen S., Warneken F. The development of prosocial behavior-from sympathy to strategy. Curr Opin Psychol. 2022. 43: 323–328.Hamlin J.K., Wynn K., Bloom P. Three-month-olds show a negativity bias in their social evaluations. Dev sci. 2010. 13 (6): 923–929.Heyes C. Where do mirror neurons come from? Neurosci Biobehav Rev. 2010. 34 (4): 575–583.Heyes C. Empathy is not in our genes. Neurosci Biobehav Rev. 2018. 95: 499–507.Heyes C., Catmur C. What happened to Mirror Neurons? Perspect Psychol Sci. 2022. 17 (1): 153–168.Hobson H.M., Bishop D.V.M. Mu suppression – A good measure of the human mirror neuron system? Cortex. 2016. 82: 290–310.Iacoboni M., Dapretto M. The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci. 2006. 7 (12): 942–51.Jauniaux J., Khatibi A., Rainville P., Jackson P.L. A meta-analysis of neuroimaging studies on pain empathy: investigating the role of visual information and observers’ perspective. Soc. Cogn. Affect Neurosci. 2019. 14 (8): 789–813.Karimova E.D., Gulyaeva A.S, Katermin N.S. The degree of mu rhythm suppression in women is associated with presence of children as well as empathy and anxiety level. Soc. Neurosci. 2022. 1–15.Kärtner J., Schuhmacher N., Collard J. Socio-cognitive influences on the domain-specificity of prosocial behavior in the second year. Infant Behav Dev. 2014. 7 (4): 665–675.Kemmerer D. What modulates the Mirror Neuron System during action observation?: Multiple factors involving the action, the actor, the observer, the relationship between actor and observer, and the context. Progr Neurobiol. 2021. 205: 102128.Kenward B., Dahl M. Preschoolers distribute scarce resources according to the moral valence of recipients’ previous actions. Dev Psychol. 2011. 47 (4): 1054–1064.Khalil R., Tindle R., Boraud T., Moustafa A.A., Karim A.A. Social decision making in autism: On the impact of mirror neurons, motor control, and imitative behaviors. CNS Neurosci Ther. 2018. 24: 669–676.Knafo-Noam A., Uzefovsk F., Israel S., Davidov M., Zahn-Waxler C. The prosocial personality and its facets: genetic and environmental architecture of mother-reported behavior of 7-year-old twins. Front psychol. 2015. 6: 112.Kochukhova O., Dyagileva Yu., Mikhailova A., Orekhova L., Makhin S., Pavlenko V. Better language – faster helper: the relation between spontaneous instrumental helping action and language ability in family-reared and institutionalized toddlers. Psychol Russia: State of the Art. 2021. 14 (4): 79–94.Kosonogov V. Why the mirror neurons cannot support action understanding. Neurophysiology. 2012. 44: 499–502.Köster M., Ohmer X., Nguyen T.D., Kärtner J. Infants understand others’ needs. Psychol Sci. 2016. 27: 542–548.Köster M., Kärtner J. Why do infants help? A simple action reveals a complex phenomenon. Developmental Rev. 2019. 51: 175–187.Köster M., Itakura S., Omori M., Kärtner J. From understanding others’ needs to prosocial action: Motor and social abilities promote infants' helping. Developmental Sci. 2019. 22: e12804.Levy J., Goldstein A., Pratt M., Feldman R. Maturation of pain empathy from child to adult shifts from single to multiple neural rhythms to support interoceptive representations. Scientific Rep. 2018. 8: 1810.Levy J., Goldstein A., Feldman R. The neural development of empathy is sensitive to caregiving and early trauma. Nat Commun. 2019. 10: 1905.Marshall P.J., Meltzoff A.N. Neural mirroring systems: exploring the EEG μ rhythm in human infancy. Dev Cogn Neurosci. 2011. 1 (2): 110–123.Marshall P.J., Meltzoff A.N. Neural mirroring mechanisms and imitation in human infant. Philos Trans R Soc Lond B Biol Sci. 2014. 369 (1644): 20130620.Meyer M., Endedijk H.M., Hunnius S. Intention to imitate: Top-down effects on 4-year-olds’ neural processing of others’ actions. Dev Cogn Neurosci. 2020. 45: 100851.Miller J.G. Physiological mechanisms of prosociality. Curr Opinion in Psychology. 2018. 20: 510–54.Mukamel R., Ekstrom A.D., Kaplan J., Iacoboni M., Fried I. Singleneuron responses in humans during execution and observation of actions. Curr Biol. 2010. 20: 750–756.Nyström P., Ljunghammar T., Rosander K., von Hofsten C. Using mu rhythm desynchronization to measure mirror neuron activity in infants. Dev Sci. 2011. 14 (2): 327–335.Olivo D., Di Ciano A., Mauro J., Giudetti L, Pampallona A., Kubera K.M., Hirjak D., Wolf R.C., Sambataro F. Neural responses of benefiting from the prosocial exchange: the effect of helping behavior. Front Psychol. 2021. 4 (12): 606858.Orekhova L.S., Makhin S.A., Mikhailova A.A., Pavlenko V.B. EEG patterns in early childhood differ between children prone to reward “Bad” or “Good” actors. Psychol Russia: State of the Art. 2020. 13 (2): 84–95.Paulus M., Moore C. Producing and understanding prosocial actions in early childhood. Adv Child Dev Behav. 2012. 42: 271–305.Paulus M., Kühn-Popp N, Licata M., Sodian B., Meinhardt J. Neural correlates of prosocial behavior in infancy: different neurophysiological mechanisms support the emergence of helping and comforting. Neuroimage. 2013. 66: 522–530.Paulus M. The emergence of prosocial behavior: Why do infants and toddlers help, comfort, and share? Child Development Perspectives. 2014. 8: 77–81.Paulus M., Rosal-Grifoll B. Helping and sharing in preschool children with autism. Exp Brain Res. 2017. 235 (7): 2081–2088.Paulus M. The multidimensional nature of early prosocial behavior: a motivational perspective. Curr Opin Psychol. 2018. 20: 111-116.Rauchbauer B., Grosbras M.H. Developmental trajectory of interpersonal motor alignment: Positive social effects and link to social cognition. Neurosci Biobehav Rev. 2020. 118: 411–425.Rizzolatti G., Sinigaglia C. The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci. 2010. 11 (4): 264–274.Saby J.N., Marshall P.J. The utility of EEG band power analysis in the study of infancy and early childhood. Dev Neuropsychol. 2012. 37: 253–273.Salo V.C., Ferrari P.F., Fox N.A. The role of the motor system in action understanding and communication: Evidence from human infants and non-human primates. Dev Psychobiol. 2019. 61 (3): 390–401.Schuhmacher N., Collard J., Kärtner J. The Differential role of parenting, peers, and temperament for explaining interindividual differences in 18-months-olds’ comforting and helping. Infant Behav Dev. 2017. 46: 124–134.Schuhmacher N., Köster M., Kärtner J. Modeling prosocial behavior increases helping in 16-month-olds. Child Dev. 2019. 90 (5): 1789–1801.Siposova B., Grueneisen S., Helming K., Tomasello M., Carpenter M. Common knowledge that help is needed increases helping behavior in children. J. Experimental. Child. Psychol. 2021. 201: 104973.Song Y., Broekhuizen M.L., Dubas J.S. Happy Little Benefactor: Prosocial Behaviors Promote Happiness in Young Children From Two Cultures. Front Psychol. 2020. 11: 1398.Southgate V. Do infants provide evidence that the mirror system is involved in action understanding? Conscious Cogn. 2013. 22 (3): 1114–1121.Steckler C.M., Liberman Z., Van de Vondervoort J.W., Slevinsky J., Le D.T., Hamlin J.K. Feeling out a link between feeling and infant sociomoral evaluation. Br. J. Dev. Psychol. 2018. 36 (3): 482–500.Stevens F., Taber K. The neuroscience of empathy and compassion in pro-social behavior. Neuropsychol. 2021. 20 (159): 107925.Svetlova M., Nichols S.R., Brownel C.A. Toddlers’ prosocial behavior: from instrumental to empathic to altruistic helping. Child Dev. 2010. 81 (6): 1814–1827.Tan E., Hamlin J.K. Infants’ neural responses to helping and hindering scenarios. Dev Cogn Neurosci. 2022. 54: 101095.Thompson E.L., Bird G., Catmur C. Conceptualizing and testing action understanding. Neurosci Biobehav Rev. 2019. 105: 106–114.Ting F., Buyukoyer Dawkins M., Stavans M., Baillargeon R. Principles and concepts in early moral cognition. In: The Social Brain: A Developmental Perspective. Ed. Decety J. Cambridge: MIT Press, 2020. 41–65 p.Tomasello M. The adaptive origins of uniquely human sociality. Philos Trans R Soc Lond B Biol Sci. 2020. 375 (1803): 20190493.Tousignant B., Eugène F., Jackson P.L. A developmental perspective on the neural bases of human empathy. Infant Behav. Dev. 2017. 48 (Pt A): 5–12.Vaish A., Carpenter M., Tomasello M. Sympathy through affective perspective taking and its relation to prosocial behavior in toddlers. Dev Psychol. 2009. 45 (2): 534–43.Varma M.M., Chen D., Lin X., Aknin L.B., Hu X. Prosocial behavior promotes positive emotion during the COVID-19 pandemic. Emotion. Advance online publication. 2022.Warneken F., Tomasello M. The roots of human altruism. Br J Psychol. 2009. 100 (Pt 3): 455–471.Warneken F. Insights into the biological foundation of human altruistic sentiments. Curr Opinion in Psychol. 2016. 7: 51–56.Warreyn P., Ruysschaert L., Wiersema J.R., Handl A., Pattyn G., Roeyers H. Infants’ mu suppression during the observation of real and mimicked goal-directed actions. Dev Sci. 2013. 16 (2): 173–185.Williamson R.A., Donohue M.R., Tully E.C. Learning how to help others: Two-year-olds’ social learning of a prosocial act. J. Exp. Child. Psychol. 2013. 114 (4): 543–550.Zahn-Waxler C., Radke-Yarrow M., Wagner E., Chapman M. Development of concern for others. Dev Psychol. 1992. 28 (1): 126–136.Zahn-Waxler C., Schoen A., Decety J. An interdisciplinary perspective on the origins of concern for others: Contributions from psychology, neuroscience, philosophy, and sociobiology. In: Forms of fellow feeling: Empathy, sympathy, concern and moral agency. Eds. Roughley N., Schramme T. Cambridge: Cambridge University Press, 2018. 184–215 p.