COOPERATIVE INFANT CALMING RESPONSE DURING MATERNAL CARRYING

 

Abstract
Mother-infant bonding is the earliest and most critical social relationship of mammalian infants. To promote this bond, infants actively send vocal signals and seek contact with their mothers, but the physiological mechanisms regulating these infant behaviors remain undefined.  Here we identify a coordinated set of infant responses during maternal carrying.  In both humans and mice, carried infants rapidly entered a calm state involving reductions in heart rate, distress vocalization, and voluntary movement.  In mouse pups, pharmacologic and genetic interventions indicated that somatosensory and proprioceptive input signaling are required for calming, and parasympathetic and cerebellar functions mediate the cardiac and motor output controls, respectively.  These findings show that infant calming is a conserved component of the mother-infant interaction, providing insight on the neural basis of social development and dysfunction.

 

Background
Mammalian parents provide intense parental care.  Infants also proactively exhibit filial attachment.
These drives are hard-wired in the mammalian brain, and postnatal learning experiences refine the actual behaviors.
The family bond experienced in early life forms the foundation of the personality and social behaviors in the future.
 
1
 
We have been studying the neural mechanism of parental behavior using laboratory mice, in which species various genetic tools are available.
 
2
(Kuroda et al, 2007, 2011)

 

Introduction
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(Brewster and Leon, 1980) 
(Eibl-Eibesfeldt, 1951)
Carrying is an important component of parental care for altricial mammals. The carried infants assume compact posture, designated as "Transport Response" by Brewster and Leon (1980).  However, scientific proof of calming effect of carrying was rather scarce.  In humans, carrying has been performed as a soothing measure, and yet the soothing effecthas been elusive in the previous literature
(Hunziker, 1986; Walker, 1994; St James-Roberts, 1995 and 2006).

 

Response to carrying: Human
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Infant (1-6 mo, N=12) movement and cry from video
Electrocardiogram 
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* nIBI : normalized inter-beat interval
(Inverse of heart rate, normalized by subjects)
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<Effect of Carrying >
Crying ↓
Voluntary movement ↓
Heart-rate ↓ (IBI ↑)

Time constant = 3.2 sec (human)
= 0.6 sec (mice) 

 

Response to carrying: Mice
<Manual carrying> <Maternal carrying>
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13
14 15
(Yoshida et al, 2013)
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<Effect of Carrying >
Crying ↓
Voluntary movement ↓
Heart-rate ↓ (IBI ↑)

Time constant = 3.2 sec (human)
= 0.6 sec (mice) 

 

Mechanism: sensory input
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Both maternal-like touch and proprioceptive information of movement are required for the infant calming response.

 

Mechanism: downstream
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Cardiac deceleration is mediated by parasympathetic activation during maternal carrying.
Immobilization is independently regulated from the autonomic nervous system.
Compact posture during carrying involves cerebellar cortex function.

 

Mechanism: nociception
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Maternal-like carrying increases apparent pain threshold in calmed infants, via a non-opioidergic mechanism.

 

Functional significance
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Infant calming response and postural regulation facilitate maternal carrying of itself.
⇒ Win-Win relationship

 

Summary of mechanisms
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Esposito G.*, Yoshida S.*, Ohnishi R., Tsuneoka Y., Rostagno MC., Yokota S., Okabe S., Kamiya K., Hoshino M., Shimizu M., Venuti P., Kikusui T., and Kato T. and Kuroda KO. : "Infant calming responses during maternal carrying in humans and mice", Current Biology, 23(9), 739-45 (2013)

*: These two authors contributed equally to this study.

Yoshida S, Esposito G, Ohnishi R, Tsuneoka Y, Okabe S, Kikusui T, Kato T, and Kuroda KO. : "Transport Response is a filial-specific behavioral response to maternal carrying in C57BL/6 mice."
Front Zool, 10(1), 50 (2013)