Brain network connectivity associated with anticipatory postural control in children and adults

Internal models provide a coherent framework for understanding motor behavior. Examples for the use of internal models include anticipatory postural adjustments (APAs), where the individual anticipates and cancels out the destabilizing effect of movement on body posture. Yet little is known about the functional changes in the brain supporting the development of APAs. Here, we addressed this issue by relating individual differences in APAs as assessed during bimanual load lifting to interindividual variation in brain network interactions at rest. We showed that the strength of the connectivity between three main canonical brain networks, namely the cingulo-opercular, the fronto-parietal and the somatosensory-motor networks, is an index of the ability to implement APAs from late childhood (9- to 11-year-old children). We also found an effect of age on the relationship between APAs and coupling strength between these networks, consistent with the notion that APAs are near but not yet fully mature in children. We discuss the implications of these findings for our understanding of learning disorders with impairment in predictive motor control.

[1]  J. Massion,et al.  Anticipatory postural changes induced by active unloading and comparison with passive unloading in man , 1982, Pflügers Archiv.

[2]  M. Hadders‐Algra,et al.  Development of postural adjustments during reaching in typically developing infants from 4 to 18 months , 2012, Experimental Brain Research.

[3]  Richard A Andersen,et al.  Forward estimation of movement state in posterior parietal cortex , 2008, Proceedings of the National Academy of Sciences.

[4]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

[5]  C. Assaiante,et al.  Independent Walking as a Major Skill for the Development of Anticipatory Postural Control: Evidence from Adjustments to Predictable Perturbations , 2013, PloS one.

[6]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[7]  D. Bassett,et al.  Emergence of system roles in normative neurodevelopment , 2015, Proceedings of the National Academy of Sciences.

[8]  S. Blakemore,et al.  Action prediction in the cerebellum and in the parietal lobe , 2003, Experimental Brain Research.

[9]  John H. Gilmore,et al.  Development of human brain cortical network architecture during infancy , 2014, Brain Structure and Function.

[10]  Richard F. Betzel,et al.  Modular Brain Networks. , 2016, Annual review of psychology.

[11]  M. Hadders‐Algra,et al.  Postural adjustments and reaching in 4- and 6-month-old infants: an EMG and kinematical study , 2007, Experimental Brain Research.

[12]  Scott T. Grafton,et al.  Role of the posterior parietal cortex in updating reaching movements to a visual target , 1999, Nature Neuroscience.

[13]  R. Ivry,et al.  Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. , 2005, Journal of neurophysiology.

[14]  M. Desmurget,et al.  A parietal-premotor network for movement intention and motor awareness , 2009, Trends in Cognitive Sciences.

[15]  Dost Öngür,et al.  Anticorrelations in resting state networks without global signal regression , 2012, NeuroImage.

[16]  Kaustubh Supekar,et al.  Dynamic Reconfiguration of Structural and Functional Connectivity Across Core Neurocognitive Brain Networks with Development , 2011, The Journal of Neuroscience.

[17]  R. Blank,et al.  Understanding performance deficits in developmental coordination disorder: a meta‐analysis of recent research , 2013, Developmental medicine and child neurology.

[18]  C. Schmitz,et al.  Development of action representation during adolescence as assessed from anticipatory control in a bimanual load-lifting task , 2012, Neuroscience.

[19]  C. Assaiante,et al.  Feedforward motor control in developmental dyslexia and developmental coordination disorder: Does comorbidity matter? , 2018, Research in developmental disabilities.

[20]  C. Schmitz,et al.  Development of anticipatory postural adjustments in a bimanual load-lifting task in children , 1999, Experimental Brain Research.

[21]  M. Hadders‐Algra,et al.  The development of postural adjustments during reaching in 6- to 18-month-old infants Evidence for two transitions , 1999, Experimental Brain Research.

[22]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[23]  Yong He,et al.  Topological organization of the human brain functional connectome across the lifespan , 2013, Developmental Cognitive Neuroscience.

[24]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[25]  John D. E. Gabrieli,et al.  Selective Development of Anticorrelated Networks in the Intrinsic Functional Organization of the Human Brain , 2014, Journal of Cognitive Neuroscience.

[26]  S. Swinnen,et al.  Dynamics of hemispheric specialization and integration in the context of motor control , 2006, Nature Reviews Neuroscience.

[27]  Jörn Diedrichsen,et al.  Cooperation Not Competition: Bihemispheric tDCS and fMRI Show Role for Ipsilateral Hemisphere in Motor Learning , 2016, The Journal of Neuroscience.

[28]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[29]  D. Wolpert,et al.  Internal models in the cerebellum , 1998, Trends in Cognitive Sciences.

[30]  Jonathan D. Power,et al.  Functional Brain Networks Develop from a “Local to Distributed” Organization , 2009, PLoS Comput. Biol..

[31]  Kaustubh Supekar,et al.  Development of Large-Scale Functional Brain Networks in Children , 2009, NeuroImage.

[32]  Sukhwinder S. Shergill,et al.  Modulation of somatosensory processing by action , 2013, NeuroImage.

[33]  C. Schmitz,et al.  Building anticipatory postural adjustment during childhood: a kinematic and electromyographic analysis of unloading in children from 4 to 8 years of age , 2002, Experimental Brain Research.

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

[35]  Jonathan D. Power,et al.  Control-related systems in the human brain , 2013, Current Opinion in Neurobiology.

[36]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[37]  Edward T. Bullmore,et al.  Network-based statistic: Identifying differences in brain networks , 2010, NeuroImage.

[38]  M. Desmurget,et al.  Movement Intention After Parietal Cortex Stimulation in Humans , 2009, Science.

[39]  R. Johansson,et al.  Evidence for the involvement of the posterior parietal cortex in coordination of fingertip forces for grasp stability in manipulation. , 2003, Journal of neurophysiology.

[40]  E. Miller,et al.  Goal-direction and top-down control , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  C. Assaiante,et al.  Boosted activation of right inferior frontoparietal network: A basis for illusory movement awareness , 2014, Human brain mapping.

[42]  N. A. Bernshteĭn The co-ordination and regulation of movements , 1967 .

[43]  Wei Gao,et al.  Functional Network Development During the First Year: Relative Sequence and Socioeconomic Correlations. , 2015, Cerebral cortex.

[44]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[45]  Joaquín Goñi,et al.  Changes in structural and functional connectivity among resting-state networks across the human lifespan , 2014, NeuroImage.

[46]  R. Johansson,et al.  Prediction Precedes Control in Motor Learning , 2003, Current Biology.

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

[48]  B. Steenbergen,et al.  Cognitive and neuroimaging findings in developmental coordination disorder: new insights from a systematic review of recent research , 2017, Developmental medicine and child neurology.

[49]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[50]  B. Steenbergen,et al.  Compromised motor control in children with DCD: A deficit in the internal model?—A systematic review , 2014, Neuroscience & Biobehavioral Reviews.

[51]  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.

[52]  J. Massion,et al.  Coordination between posture and movement in a bimanual load lifting task: putative role of a medial frontal region including the supplementary motor area , 2004, Experimental Brain Research.

[53]  J. Massion,et al.  Acquisition of anticipatory postural adjustments in a bimanual load-lifting task: normal and pathological aspects , 1999, Experimental Brain Research.

[54]  M. Hadders‐Algra,et al.  The Development of Postural Response Patterns During Reaching in Healthy Infants , 1998, Neuroscience & Biobehavioral Reviews.

[55]  Christos Davatzikos,et al.  Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity , 2017, NeuroImage.

[56]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[57]  Jonathan D. Power,et al.  Multi-task connectivity reveals flexible hubs for adaptive task control , 2013, Nature Neuroscience.

[58]  Paul F. Sowman,et al.  Neuromagnetic brain activity associated with anticipatory postural adjustments for bimanual load lifting , 2013, NeuroImage.