Mother brain is wired for social moments
- Ortal Shimon-Raz
- Roy Salomon
- Miki Bloch
- Gabi Aisenberg Romano
- Yaara Yeshurun
- Adi Ulmer-Yaniv
- Orna Zagoory-Sharon
- Ruth Feldman
- IDC Herzliya, Israel
- Bar Ilan University, Israel
- Tel Aviv Sourasky Medical Center, Israel
- Tel Aviv University, Israel
Abstract
Reorganization of the maternal brain upon childbirth triggers species-typical maternal social behavior. These brief social moments carry profound effects on the infant's brain and likely have distinct signature in the maternal brain. Utilizing a double-blind, within-subject oxytocin/placebo administration crossover design, mothers' brain was imaged twice using fMRI while observing three naturalistic maternal-infant contexts in the home ecology; 'unavailable', 'unresponsive', and 'social', when mothers engaged in synchronous peek-a-boo play. The social condition elicited greater neural response across the human caregiving network, including amygdala, VTA, hippocampus, insula, ACC, and temporal cortex. Oxytocin impacted neural response primarily to the social condition and attenuated differences between social and non-social stimuli. Greater temporal consistency emerged in the 'social' condition across the two imaging sessions, particularly in insula, amygdala, and TP. Findings describe how mother's brain varies by caregiving experiences and gives salience to moments of social synchrony that support infant social development and brain maturation.
Data availability
We shared raw, subject by subject, anonymized brain data (fMRI); group level data (e.g. unthresholded group maps on MNI template) and raw subject by subject data from the ROI analysis (csv and JASP files). These files are uploaded to our OSF account (https://osf.io/mszqj/?view_only=0daf10c02c984ead8929452edf44e550). We believe that these measures will allow full transparency of the data.
Article and author information
Author details
Funding
Simms/Mann Foundation
- Ruth Feldman
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Alexander Shackman, University of Maryland, United States
Ethics
Human subjects: The study was approved by the Bar-Ilan University's IRB and by the Helsinki committee of the Sourasky medical center, Tel Aviv (Ethical approval no. 0161-14-TLV). All participants signed an informed consent.
Version history
- Received: May 28, 2020
- Accepted: March 22, 2021
- Accepted Manuscript published: March 25, 2021 (version 1)
- Version of Record published: April 7, 2021 (version 2)
Copyright
© 2021, Shimon-Raz et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 2,625
- views
-
- 313
- downloads
-
- 18
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Mother brain is wired for social moments
eLife 10:e59436.
https://doi.org/10.7554/eLife.59436
Further reading
-
- Neuroscience
The brain’s ability to appraise threats and execute appropriate defensive responses is essential for survival in a dynamic environment. Humans studies have implicated the anterior insular cortex (aIC) in subjective fear regulation and its abnormal activity in fear/anxiety disorders. However, the complex aIC connectivity patterns involved in regulating fear remain under investigated. To address this, we recorded single units in the aIC of freely moving male mice that had previously undergone auditory fear conditioning, assessed the effect of optogenetically activating specific aIC output structures in fear, and examined the organization of aIC neurons projecting to the specific structures with retrograde tracing. Single-unit recordings revealed that a balanced number of aIC pyramidal neurons’ activity either positively or negatively correlated with a conditioned tone-induced freezing (fear) response. Optogenetic manipulations of aIC pyramidal neuronal activity during conditioned tone presentation altered the expression of conditioned freezing. Neural tracing showed that non-overlapping populations of aIC neurons project to the amygdala or the medial thalamus, and the pathway bidirectionally modulated conditioned fear. Specifically, optogenetic stimulation of the aIC-amygdala pathway increased conditioned freezing, while optogenetic stimulation of the aIC-medial thalamus pathway decreased it. Our findings suggest that the balance of freezing-excited and freezing-inhibited neuronal activity in the aIC and the distinct efferent circuits interact collectively to modulate fear behavior.
-
- Neuroscience
Motor learning is often viewed as a unitary process that operates outside of conscious awareness. This perspective has led to the development of sophisticated models designed to elucidate the mechanisms of implicit sensorimotor learning. In this review, we argue for a broader perspective, emphasizing the contribution of explicit strategies to sensorimotor learning tasks. Furthermore, we propose a theoretical framework for motor learning that consists of three fundamental processes: reasoning, the process of understanding action–outcome relationships; refinement, the process of optimizing sensorimotor and cognitive parameters to achieve motor goals; and retrieval, the process of inferring the context and recalling a control policy. We anticipate that this ‘3R’ framework for understanding how complex movements are learned will open exciting avenues for future research at the intersection between cognition and action.
