Frequency of Maternal Touch Predicts Resting Activity and Connectivity of the Developing Social Brain

Cerebral Cortex, August 2016;26: 3544–3552 doi:10.1093/cercor/bhw137 Advance Access Publication Date: 26 May 2016 Original Article ORIGINAL ARTICLE Frequency of Maternal Touch Predicts Resting Activity and Connectivity of the Developing Social Brain Jens Brauer1, Yaqiong Xiao1, Tanja Poulain2, Angela D. Friederici1 and Annett Schirmer3,4,5 Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, 2LIFE Research Center, University of Leipzig, Leipzig, Germany, 3Department of Psychology and 4LSI Neurobiology/Ageing Programme, National University of Singapore, Singapore, Singapore and 5Duke/NUS Graduate Medical School, Singapore, Singapore Address correspondence to Jens Brauer, Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1A, 04103 Leipzig, Germany. Email: ; Annett Schirmer, National University of Singapore, 9 Arts Link, Block AS4, Level 2, Singapore 117570, Singapore. Email: Abstract Previous behavioral research points to a positive relationship between maternal touch and early social development. Here, we explored the brain correlates of this relationship. The frequency of maternal touch was recorded for 43 five-year-old children during a 10 min standardized play session. Additionally, all children completed a resting-state functional magnetic resonance imaging session. Investigating the default mode network revealed a positive relation between the frequency of maternal touch and activity in the right posterior superior temporal sulcus (pSTS) extending into the temporo-parietal junction. Using this effect as a seed in a functional connectivity analysis identified a network including extended bilateral regions along the temporal lobe, bilateral frontal cortex, and left insula. Compared with children with low maternal touch, children with high maternal touch showed additional connectivity with the right dorso-medial prefrontal cortex. Together these results support the notion that childhood tactile experiences shape the developing “social brain” with a particular emphasis on a network involved in mentalizing. Key words: affective touch, C-tactile afferents, resting-state fMRI, stroking, theory of mind Introduction Touch powerfully communicates emotions and contributes to the formation of social bonds (Suvilehto et al. 2015). As such it plays an important role in parent–child interactions and early attachment formation. Here, we explored whether the touch parents direct at their children has effects beyond social bonding and shapes functional aspects of the developing brain. More specifically, we asked whether and how the frequency of parental touch predicts children’s engagement of brain structures known to contribute to the “social brain.” The term “social brain” describes neuronal networks enabling our dealings with the social world. Specifically, our interest in others, our sensitivity to their emotions, thoughts, and intentions, and our ability to meaningfully interact with them are presumably supported by dedicated brain processes separate from those supporting our dealings with the inanimate world (Dunbar and Shultz 2007; Frith 2007; Adolphs 2009). Many structures, including posterior superior temporal cortex ( pSTS), temporoparietial junction (TPJ), and medial prefrontal cortex (mPFC), were identified as contributing to the “social brain” (Schirmer and Kotz 2006; Frith 2007; Van Overwalle 2009; Kennedy and Adolphs 2012; © The Author 2016. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact 1 Touch and the Developing Social Brain | 3545 To this end, we invited 5-year-old children and their mothers to participate in a behavioral and a neuroimaging session. The behavioral session comprised a 10-min observational period during which children played with their mothers and for which we recorded the frequency of maternal and child touch. During the neuroimaging session, we subjected children to functional magnetic resonance imaging (fMRI) as to measure their brain activity during wakeful rest. Here, our focus was on 2 variables referred to as regional homogeneity (ReHo) and resting-state functional connectivity (RSFC). ReHo reflects local temporal synchronization in the spontaneous activity of nearest neighbor voxels in fMRI time series (for further details, see Materials and Methods). It sheds light on the so-called “default mode network” (DMN, Long et al. 2008)— a distributed set of brain regions that are active when participants are wakefully at rest but suppressed when they perform a task (Shulman et al. 1997; Gusnard and Raichle 2001; Raichle et al. 2001). Regions contributing to the DMN include medial structures such as mPFC, the medial temporal lobe, as well as the posterior cingulate cortex, but also more lateral areas such as the inferior parietal lobule (IPL), TPJ, and temporal poles. As such there is much anatomical overlap between the DMN and the “social brain” (Mars et al. 2012). Moreover, many studies have linked DMN activity to social functioning (for reviews, see MolnarSzakacs and Uddin 2013; Li et al. 2014). Apart from the DMN, resting-state research identified several other networks that mirror task-related activity and are referred to as task-positive. Using an RSFC approach, it was shown that certain regions supporting a particular motor or mental function slowly oscillate together when participants are without a task (Biswal et al. 1995; Deco and Corbetta 2011). For example, temporal regions identified by contrasting the visual encoding of people versus nonsocial objects were found to remain functionally connected after the task through slow oscillations in blood oxygenation (Simmons et al. 2010). Like DMN activity, RSFC was shown to predict performance in social paradigms (Zhu et al. 2011; Takeuchi et al. 2013, 2014). Against the background of these findings, the present study tested the following hypotheses. First, we expected the frequency of maternal touch to predict resting-state activity in nodes overlapping with the “social brain.” Moreover, of particular interest were insula and pSTS as their activity is directly modulated by tactile input. Second, we predicted that touch-dependent DMN effects have knock-on consequences for RSFC. Specifically, such consequences should emerge for regions implicated in social tasks like those that require mentalizing. Materials and Methods Participants Fifty-five mother–child dyads were invited to participate in the study. Two of these children did not pass the mock scanner session and therefore did not enter the MR part of this study. Six children undergoing real MRI scanning failed to complete the scanning (...truncated)