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

Previous behavioral research points to a positive relationship between maternal touch and early social development. Here, we explored the brain correlatesof this relationship. The frequencyofmaternal touchwas recorded for 43five-year-old childrenduring a 10min 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 ofmaternal 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.

[1]  B. Egeland,et al.  Infant-mother attachment: factors related to its development and changes over time. , 1984, Child development.

[2]  M. Ainsworth,et al.  Attachment as Related to Mother-Infant Interaction , 1979 .

[3]  A. R. Muir,et al.  The structure and function of a slowly adapting touch corpuscle in hairy skin , 1969, The Journal of physiology.

[4]  David J. Anderson,et al.  Genetic identification of C-fibers that detect massage-like stroking of hairy skin in vivo , 2012, Nature.

[5]  Xi-Nian Zuo,et al.  REST: A Toolkit for Resting-State Functional Magnetic Resonance Imaging Data Processing , 2011, PloS one.

[6]  Daniel D. Dilks,et al.  Resting-State Neural Activity across Face-Selective Cortical Regions Is Behaviorally Relevant , 2011, The Journal of Neuroscience.

[7]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[8]  Xu Wang,et al.  Neural correlates of psychological resilience and their relation to life satisfaction in a sample of healthy young adults , 2015, NeuroImage.

[9]  R. Heslin,et al.  Hands touching hands: affective and evaluative effects of an interpersonal touch. , 1976, Sociometry.

[10]  Daniel S. Margulies,et al.  Longitudinal changes in resting-state fMRI from age 5 to age 6 years covary with language development , 2016, NeuroImage.

[11]  S. Hofmann,et al.  Children's emotion understanding: A meta-analysis of training studies. , 2015, Developmental review : DR.

[12]  S. Kotz,et al.  Beyond the right hemisphere: brain mechanisms mediating vocal emotional processing , 2006, Trends in Cognitive Sciences.

[13]  W. K. Simmons,et al.  The Selectivity and Functional Connectivity of the Anterior Temporal Lobes , 2009, Cerebral cortex.

[14]  Yufeng Zang,et al.  Toward reliable characterization of functional homogeneity in the human brain: Preprocessing, scan duration, imaging resolution and computational space , 2013, NeuroImage.

[15]  M. Corbetta,et al.  The Dynamical Balance of the Brain at Rest , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[16]  Robin I. M. Dunbar,et al.  Topography of social touching depends on emotional bonds between humans , 2015, Proceedings of the National Academy of Sciences.

[17]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[18]  Ivan Toni,et al.  On the relationship between the “default mode network” and the “social brain” , 2012, Front. Hum. Neurosci..

[19]  K. Pelphrey,et al.  Autistic traits are associated with diminished neural response to affective touch. , 2013, Social cognitive and affective neuroscience.

[20]  F. Overwalle.  Social cognition and the brain: a meta-analysis. , 2009 .

[21]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[22]  Robin I. M. Dunbar,et al.  Evolution of the Social Brain , 2003, Science.

[23]  V. Calhoun,et al.  Specific default mode subnetworks support mentalizing as revealed through opposing network recruitment by social and semantic FMRI tasks , 2015, Human brain mapping.

[24]  Wanqing Li,et al.  The default mode network and social understanding of others: what do brain connectivity studies tell us , 2014, Front. Hum. Neurosci..

[25]  A. Sandler,et al.  Comparison of skin-to-skin (Kangaroo) and traditional care: Parenting outcomes and preterm infant development. , 2003 .

[26]  G. McCarthy,et al.  Neural basis of eye gaze processing deficits in autism. , 2005, Brain : a journal of neurology.

[27]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[28]  Matthew J. Hertenstein,et al.  The tactile context of a mother’s caregiving: implications for attachment of low birth weight infants☆ , 2000 .

[29]  S. Weiss.  Haptic perception and the psychosocial functioning of preterm, low birth weight infants , 2005 .

[30]  J. Watt.  Interaction, intervention, and development in small-for-gestational-age infants , 1990 .

[31]  J. Wessberg,et al.  Discriminative and Affective Touch: Sensing and Feeling , 2014, Neuron.

[32]  F. Champagne,et al.  The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care , 2005, Neuroscience & Biobehavioral Reviews.

[33]  Malin Björnsdotter,et al.  Development of brain mechanisms for processing affective touch , 2014, Front. Behav. Neurosci..

[34]  Yufeng Zang,et al.  Regional homogeneity of resting state fMRI signals predicts Stop signal task performance , 2012, NeuroImage.

[35]  J. Wessberg,et al.  Human C-Tactile Afferents Are Tuned to the Temperature of a Skin-Stroking Caress , 2014, The Journal of Neuroscience.

[36]  Daniel P. Kennedy,et al.  A specific hypoactivation of right temporo-parietal junction/posterior superior temporal sulcus in response to socially awkward situations in autism. , 2015, Social cognitive and affective neuroscience.

[37]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[38]  T. Field,et al.  Preterm infant massage therapy research: a review. , 2010, Infant behavior & development.

[39]  Tianzi Jiang,et al.  Regional homogeneity of the resting-state brain activity correlates with individual intelligence , 2011, Neuroscience Letters.

[40]  M. Kimura,et al.  Inactivation of the putamen selectively impairs reward history-based action selection , 2011, Experimental Brain Research.

[41]  Mark A. Elliott,et al.  Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth , 2012, NeuroImage.

[42]  Gustavo Turecki,et al.  Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse , 2009, Nature Neuroscience.

[43]  J. Wessberg,et al.  Coding of pleasant touch by unmyelinated afferents in humans , 2009, Nature Neuroscience.

[44]  E Anisfeld,et al.  Does infant carrying promote attachment? An experimental study of the effects of increased physical contact on the development of attachment. , 1990, Child development.

[45]  D. Muir,et al.  Adult tactile stimulation during face-to-face interactions modulates five-month-olds' affect and attention. , 1992, Child development.

[46]  Wei Liao,et al.  The synchronization of spontaneous BOLD activity predicts extraversion and neuroticism , 2011, Brain Research.

[47]  Didier Grandjean,et al.  On the spatial organization of sound processing in the human temporal lobe: A meta-analysis , 2012, NeuroImage.

[48]  R. Ebstein,et al.  Maternal touch predicts social orienting in young children , 2016 .

[49]  Anqi Qiu,et al.  Emotional expressions in voice and music: Same code, same effect? , 2013, Human brain mapping.

[50]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[51]  Shakti Sharma,et al.  Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. , 1997, Science.

[52]  C. Frith.  The social brain? , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  Hedda Lausberg,et al.  Methods in Gesture Research: , 2009 .

[54]  A. Friederici,et al.  Development of a selective left-hemispheric fronto-temporal network for processing syntactic complexity in language comprehension , 2016, Neuropsychologia.

[55]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[56]  Helen E. Fisher,et al.  Romantic love: An fMRI study of a neural mechanism for mate choice , 2005, The Journal of comparative neurology.

[57]  U. Frith,et al.  Annual research review: Towards a developmental neuroscience of atypical social cognition. , 2014, Journal of child psychology and psychiatry, and allied disciplines.

[58]  A. Iggo,et al.  Cutaneous mechanoreceptors with afferent C fibres , 1960, The Journal of physiology.

[59]  Danielle Z. Bolling,et al.  Brain mechanisms for processing affective touch , 2013, Human brain mapping.

[60]  Sarah M. Tashjian,et al.  Beyond Sally's missing marble: further development in children's understanding of mind and emotion in middle childhood. , 2015, Advances in child development and behavior.

[61]  D. Louis Collins,et al.  Unbiased average age-appropriate atlases for pediatric studies , 2011, NeuroImage.

[62]  Pascal Belin,et al.  People-selectivity, audiovisual integration and heteromodality in the superior temporal sulcus , 2014, Cortex.

[63]  Yasuyuki Taki,et al.  Resting state functional connectivity associated with trait emotional intelligence , 2013, NeuroImage.

[64]  Michael J Meaney,et al.  Epigenetic programming by maternal behavior , 2004, Nature Neuroscience.

[65]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[66]  Daniel P. Kennedy,et al.  The social brain in psychiatric and neurological disorders , 2012, Trends in Cognitive Sciences.

[67]  D. Stack,et al.  Investigating Maternal Touch and Infants' Self-Regulatory Behaviours during a Modified Face-to-Face Still-Face with Touch Procedure. , 2014 .

[68]  Shakti Sharma,et al.  Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Tiffany M Field,et al.  Infants' preference for touch stimulation in face-to-face interactions , 1996 .

[70]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[71]  Yong He,et al.  Addressing head motion dependencies for small-world topologies in functional connectomics , 2013, Front. Hum. Neurosci..

[72]  Liang Wang,et al.  Default mode network as revealed with multiple methods for resting-state functional MRI analysis , 2008, Journal of Neuroscience Methods.

[73]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[74]  Chaogan Yan,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010, Front. Syst. Neurosci..

[75]  Mark H Johnson,et al.  The emergence of the social brain network: Evidence from typical and atypical development , 2005, Development and Psychopathology.

[76]  K. Grossmann,et al.  Maternal sensitivity and newborns' orientation responses as related to quality of attachment in northern Germany. , 1985, Monographs of the Society for Research in Child Development.

[77]  R. Adolphs,et al.  The social brain: neural basis of social knowledge. , 2009, Annual review of psychology.

[78]  S. Swinnen,et al.  Underconnectivity of the superior temporal sulcus predicts emotion recognition deficits in autism. , 2014, Social cognitive and affective neuroscience.

[79]  M. Dapretto,et al.  Reading affect in the face and voice: neural correlates of interpreting communicative intent in children and adolescents with autism spectrum disorders. , 2007, Archives of general psychiatry.

[80]  Danielle Z. Bolling,et al.  fNIRS detects temporal lobe response to affective touch. , 2014, Social cognitive and affective neuroscience.

[81]  Béatrice de Gelder,et al.  Lateralization for dynamic facial expressions in human superior temporal sulcus , 2015, NeuroImage.

[82]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[83]  Y. Lamarre,et al.  Unmyelinated tactile afferents signal touch and project to insular cortex , 2002, Nature Neuroscience.

[84]  Istvan Molnar-Szakacs,et al.  Self-Processing and the Default Mode Network: Interactions with the Mirror Neuron System , 2013, Front. Hum. Neurosci..

[85]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[86]  Elina Pihko,et al.  Development of Human Somatosensory Cortical Functions – What have We Learned from Magnetoencephalography: A Review , 2014, Front. Hum. Neurosci..

[87]  Francis McGlone,et al.  Brain Mechanisms for Processing Affective (and Nonaffective) Touch Are Atypical in Autism. , 2016, Cerebral cortex.

[88]  Simone Kühn,et al.  The neural basis of unwanted thoughts during resting state. , 2014, Social cognitive and affective neuroscience.

[89]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[90]  Bharat B. Biswal,et al.  The oscillating brain: Complex and reliable , 2010, NeuroImage.

[91]  C. Kelly,et al.  Age-related changes in intrinsic function of the superior temporal sulcus in autism spectrum disorders. , 2015, Social cognitive and affective neuroscience.