Infant Calming Responses during Maternal Carrying in Humans and Mice

¹ Unit for Affiliative Social Behavior, RIKEN Brain Science Institute, Wako-shi, Saitama 351-0198, Japan
² Laboratory for Molecular Dynamics of Mental Disorders, RIKEN Brain Science Institute, Wako-shi, Saitama 351-0198, Japan
³ Department of Psychology and Cognitive Science, University of Trento, Rovereto, Trento 38068, Italy
⁴ Department of Clinical Laboratory, Saitama Children’s Medical Center, Saitama-shi, Saitama 339-8551, Japan
⁵ Division of Neonatology, Saitama Children’s Medical Center, Saitama-shi, Saitama 339-8551, Japan
⁶ Companion Animal Research, School of Veterinary Medicine, Azabu University, Sagamihara-shi, Kanagawa 252-5201 Japan
⁷ Department of Otorhinolaryngology, Juntentdo University School of Medicine, Bunkyo-ku, Tokyo 113-8421, Japan
⁸ Department of Biochemistry and Cellular Biology, National Institute of Neuroscience, National Center of Neurology and Psychiatry, Kodaira-shi, Tokyo 187-8551, Japan

http://dx.doi.org/10.1016/j.cub.2013.03.041, How to Cite or Link Using DOI

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Summary

Background

Mother-infant bonding is the earliest and most critical social relationship of mammalian infants. To promote this bond, infants have innate behaviors to seek maternal proximity and protest upon separation via communication with the mother vocally and through body movement. However, the physiological mechanisms regulating these infant behaviors remain largely undefined.

Results

Here we show a novel set of infant cooperative responses during maternal carrying. Infants under 6 months of age carried by a walking mother immediately stopped voluntary movement and crying and exhibited a rapid heart rate decrease, compared with holding by a sitting mother. Furthermore, we identified strikingly similar responses in mouse pups as defined by immobility and diminished ultrasonic vocalizations and heart rate. Using pharmacologic and genetic interventions in mouse pups, we identified the upstream and downstream neural systems regulating the calming response. Somatosensory and proprioceptive input signaling are required for induction, and parasympathetic and cerebellar functions mediate cardiac and motor output, respectively. The loss of the calming response hindered maternal rescue of the pups, suggesting a functional significance for the identified calming response.

Conclusions

Our study has demonstrated for the first time that the infant calming response to maternal carrying is a coordinated set of central, motor, and cardiac regulations and is a conserved component of mammalian mother-infant interactions. Our findings provide evidence for and have the potential to impact current parenting theory and practice, since unsoothable crying is the major risk factor for child abuse.