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Research Article

Neurobiology of culturally common maternal responses to infant cry

Marc H. Bornstein, View ORCID ProfileDiane L. Putnick, Paola Rigo, Gianluca Esposito, James E. Swain, Joan T. D. Suwalsky, Xueyun Su, Xiaoxia Du, Kaihua Zhang, Linda R. Cote, Nicola De Pisapia, and Paola Venuti
PNAS November 7, 2017 114 (45) E9465-E9473; first published October 23, 2017; https://doi.org/10.1073/pnas.1712022114
Marc H. Bornstein
aChild and Family Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892;
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  • For correspondence: Marc_H_Bornstein@nih.gov
Diane L. Putnick
aChild and Family Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892;
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  • ORCID record for Diane L. Putnick
Paola Rigo
aChild and Family Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892;
bDepartment of Psychology and Cognitive Science, University of Trento, I-38068 Trento, Italy;
cDivision of Psychology, Nanyang Technological University, Singapore 639798;
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Gianluca Esposito
bDepartment of Psychology and Cognitive Science, University of Trento, I-38068 Trento, Italy;
cDivision of Psychology, Nanyang Technological University, Singapore 639798;
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James E. Swain
dStony Brook University Hospital Medical Center, Stony Brook, NY 11794;
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Joan T. D. Suwalsky
aChild and Family Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD 20892;
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Xueyun Su
eEast China Normal University, Shanghai 200241, China;
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Xiaoxia Du
eEast China Normal University, Shanghai 200241, China;
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Kaihua Zhang
eEast China Normal University, Shanghai 200241, China;
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Linda R. Cote
fDepartment of Psychology, Marymount University, Arlington, VA 22207
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Nicola De Pisapia
bDepartment of Psychology and Cognitive Science, University of Trento, I-38068 Trento, Italy;
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Paola Venuti
bDepartment of Psychology and Cognitive Science, University of Trento, I-38068 Trento, Italy;
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  1. Edited by Charles Gross, Princeton University, Princeton, NJ, and approved September 6, 2017 (received for review July 7, 2017)

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Significance

We undertook an interdisciplinary exploration that unites evolutionary biology, neuroscience, and developmental cultural psychology. Based on extensive and detailed behavioral analyses of 684 new mothers in 11 countries and complementary functional magnetic resonance imaging (fMRI) analyses of brain responses in 43 first-time new US mothers to their own infants’ cries, 44 experienced Chinese mothers to infant cries and control emotional sounds, and 12 Italian mothers and nonmothers to generic infant cries, we identified specific behavior repertoires and specific corresponding activated brain regions in human caregivers that constitute primary responses to infant distress. This study set will appeal to scientific and general audiences because it elucidates the foundations of core parenting practices in response to infant vocal distress.

Abstract

This report coordinates assessments of five types of behavioral responses in new mothers to their own infants’ cries with neurobiological responses in new mothers to their own infants’ cries and in experienced mothers and inexperienced nonmothers to infant cries and other emotional and control sounds. We found that 684 new primipara mothers in 11 countries (Argentina, Belgium, Brazil, Cameroon, France, Kenya, Israel, Italy, Japan, South Korea, and the United States) preferentially responded to their infants’ vocalizing distress by picking up and holding and by talking to their infants, as opposed to displaying affection, distracting, or nurturing. Complementary functional magnetic resonance imaging (fMRI) analyses of brain responses to their own infants’ cries in 43 new primipara US mothers revealed enhanced activity in concordant brain territories linked to the intention to move and to speak, to process auditory stimulation, and to caregive [supplementary motor area (SMA), inferior frontal regions, superior temporal regions, midbrain, and striatum]. Further, fMRI brain responses to infant cries in 50 Chinese and Italian mothers replicated, extended, and, through parcellation, refined the results. Brains of inexperienced nonmothers activated differently. Culturally common responses to own infant cry coupled with corresponding fMRI findings to own infant and to generic infant cries identified specific, common, and automatic caregiving reactions in mothers to infant vocal expressions of distress and point to their putative neurobiological bases. Candidate behaviors embedded in the nervous systems of human caregivers lie at the intersection of evolutionary biology and developmental cultural psychology.

  • maternal responsiveness
  • neurobiology
  • culture
  • infant cry
  • fMRI

Footnotes

  • ↵1To whom correspondence should be addressed. Email: Marc_H_Bornstein{at}nih.gov.
  • Author contributions: M.H.B., P.R., G.E., J.T.D.S., and P.V. designed research; M.H.B., P.R., G.E., J.E.S., J.T.D.S., X.S., D.X., K.Z., L.R.C., N.D.P., and P.V. performed research; D.L.P., P.R., J.E.S., L.R.C., and N.D.P. analyzed data; and M.H.B., D.L.P., and P.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1712022114/-/DCSupplemental.

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Culturally common maternal responses to infant cry
Marc H. Bornstein, Diane L. Putnick, Paola Rigo, Gianluca Esposito, James E. Swain, Joan T. D. Suwalsky, Xueyun Su, Xiaoxia Du, Kaihua Zhang, Linda R. Cote, Nicola De Pisapia, Paola Venuti
Proceedings of the National Academy of Sciences Nov 2017, 114 (45) E9465-E9473; DOI: 10.1073/pnas.1712022114

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Culturally common maternal responses to infant cry
Marc H. Bornstein, Diane L. Putnick, Paola Rigo, Gianluca Esposito, James E. Swain, Joan T. D. Suwalsky, Xueyun Su, Xiaoxia Du, Kaihua Zhang, Linda R. Cote, Nicola De Pisapia, Paola Venuti
Proceedings of the National Academy of Sciences Nov 2017, 114 (45) E9465-E9473; DOI: 10.1073/pnas.1712022114
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