Title: Dissociating instructive and reorganizing effects of experience on development of 1 human

Comparisons across adults with different sensory histories (blind vs. sighted) have uncovered effects of experience on the development of human brain function. In people born blind visual cortices become responsive to non-visual tasks and show enhanced functional coupling with fronto-parietal executive systems at rest. Little is known about the developmental origins of experience-based plasticity in humans, since almost all research has been done with adults. Here we take a new approach by comparing resting state data across blind (n=30) and blindfolded sighted (n=50) adults to two large cohorts of sighted infants (dHCP, n=327, n=475). By comparing the infant “starting state” to adult outcomes, we dissociate the instructive role of vision from reorganization due to blindness. As previously reported, we find that in sighted adults, visual networks show stronger functional coupling with other sensory-motor networks (i.e., auditory, somatosensory) than with higher-cognitive prefrontal networks at rest. By contrast, visual cortices of adults born blind show the opposite pattern: stronger functional connectivity with higher-cognitive prefrontal networks. Remarkably, we find that the connectivity profile of secondary visual cortices in infants resembles that of blind more than sighted adults. Visual experience appears to ‘instruct’ coupling of visual cortex with other sensory-motor networks and de-couple from prefrontal systems. By contrast primary visual cortex (V1) shows a mixture of instructive effects of vision and reorganizing effects of blindness. Finally, lateralization of occipital connectivity appears to be driven by blindness-related reorganization, since infants resembles sighted adults. These results reveal instructive and reorganizing effect of experience on functional connectivity of human cortex.

[1]  Elizabeth J. Saccone,et al.  Sensory Modality and Spoken Language Shape Reading Network in Blind Readers of Braille , 2021, bioRxiv.

[2]  L. Naci,et al.  Typical and disrupted brain circuitry for conscious awareness in full-term and preterm infants , 2021, bioRxiv.

[3]  M. Bedny,et al.  ‘Visual’ cortices of congenitally blind adults are sensitive to response selection demands in a go/no-go task , 2021, NeuroImage.

[4]  B. Röder,et al.  Visual experience dependent plasticity in humans , 2020, Current Opinion in Neurobiology.

[5]  B. Wandell,et al.  V1 Projection Zone Signals in Human Macular Degeneration Depend on Task Despite Absence of Visual Stimulus , 2020, Current Biology.

[6]  H. Luhmann,et al.  Transient cortical circuits match spontaneous and sensory-driven activity during development , 2020, Science.

[7]  B. Röder,et al.  Sensory experience during early sensitive periods shapes cross-modal temporal biases , 2020, eLife.

[8]  B. Kolb,et al.  Critical period regulation across multiple timescales , 2020, Proceedings of the National Academy of Sciences.

[9]  M. Ashtari,et al.  Compensatory Cross-Modal Plasticity Persists After Sight Restoration , 2020, Frontiers in Neuroscience.

[10]  Daniel Rueckert,et al.  The developing Human Connectome Project (dHCP) automated resting-state functional processing framework for newborn infants , 2019, NeuroImage.

[11]  L. Cohen,et al.  Distinctive Interaction Between Cognitive Networks and the Visual Cortex in Early Blind Individuals. , 2019, Cerebral cortex.

[12]  Dinggang Shen,et al.  Resting-state functional MRI studies on infant brains: A decade of gap-filling efforts , 2019, NeuroImage.

[13]  L. Cohen,et al.  Distinctive interaction between cognitive networks and the visual cortex in early blind individuals , 2018, bioRxiv.

[14]  Evan M. Gordon,et al.  Local-Global Parcellation of the Human Cerebral Cortex From Intrinsic Functional Connectivity MRI , 2017, bioRxiv.

[15]  Connor Lane,et al.  Reduced Left Lateralization of Language in Congenitally Blind Individuals , 2017, Journal of Cognitive Neuroscience.

[16]  J. Pillai.  Functional Connectivity. , 2017, Neuroimaging clinics of North America.

[17]  L. Feigenson,et al.  Absence of visual experience modifies the neural basis of numerical thinking , 2016, Proceedings of the National Academy of Sciences.

[18]  Yufeng Zang,et al.  DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging , 2016, Neuroinformatics.

[19]  Ehud Zohary,et al.  The Limits of Shape Recognition following Late Emergence from Blindness , 2015, Current Biology.

[20]  M. Bedny,et al.  “Visual” Cortex of Congenitally Blind Adults Responds to Syntactic Movement , 2015, The Journal of Neuroscience.

[21]  B. Röder,et al.  The effect of early visual deprivation on the neural bases of multisensory processing. , 2015, Brain : a journal of neurology.

[22]  A. Caramazza,et al.  Functional connectivity of visual cortex in the blind follows retinotopic organization principles , 2015, Brain : a journal of neurology.

[23]  Birk Diedenhofen,et al.  cocor: A Comprehensive Solution for the Statistical Comparison of Correlations , 2015, PloS one.

[24]  B. Biswal.  Resting-State Functional Connectivity , 2015 .

[25]  M. Raichle,et al.  Resting state functional connectivity in early blind humans , 2014, Front. Syst. Neurosci..

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

[27]  D. Maurer,et al.  The effect of early visual deprivation on the development of face detection. , 2013, Developmental science.

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

[29]  M. Stryker,et al.  Development and Plasticity of the Primary Visual Cortex , 2012, Neuron.

[30]  Nicola Filippini,et al.  Language networks in anophthalmia: maintained hierarchy of processing in 'visual' cortex. , 2012, Brain : a journal of neurology.

[31]  Harold Burton,et al.  Recognition memory for Braille or spoken words: An fMRI study in early blind , 2012, Brain Research.

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

[33]  Daniel N. Hill,et al.  Development of Direction Selectivity in Mouse Cortical Neurons , 2011, Neuron.

[34]  R. Saxe,et al.  Language processing in the occipital cortex of congenitally blind adults , 2011, Proceedings of the National Academy of Sciences.

[35]  G. Vandewalle,et al.  Functional specialization for auditory–spatial processing in the occipital cortex of congenitally blind humans , 2011, Proceedings of the National Academy of Sciences.

[36]  F. Turkheimer,et al.  Emergence of resting state networks in the preterm human brain , 2010, Proceedings of the National Academy of Sciences.

[37]  C. Büchel,et al.  Corticocortical Connections Mediate Primary Visual Cortex Responses to Auditory Stimulation in the Blind , 2010, The Journal of Neuroscience.

[38]  D. Schacter,et al.  Correlated low-frequency BOLD fluctuations in the resting human brain are modulated by recent experience in category-preferential visual regions. , 2010, Cerebral cortex.

[39]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[40]  Peter Fransson,et al.  Spontaneous Brain Activity in the Newborn Brain During Natural Sleep—An fMRI Study in Infants Born at Full Term , 2009, Pediatric Research.

[41]  Dinggang Shen,et al.  Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects , 2009, Proceedings of the National Academy of Sciences.

[42]  Kevin G. Guise,et al.  Functional connectivity of the sensorimotor area in naturally sleeping infants , 2008, Brain Research.

[43]  Chunshui Yu,et al.  Altered functional connectivity of primary visual cortex in early blindness , 2008, Human brain mapping.

[44]  Chunshui Yu,et al.  Whole brain functional connectivity in the early blind. , 2007, Brain : a journal of neurology.

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

[46]  D. Maurer,et al.  Effects of early visual deprivation on perceptual and cognitive development. , 2007, Progress in brain research.

[47]  D. Fitzpatrick,et al.  The development of direction selectivity in ferret visual cortex requires early visual experience , 2006, Nature Neuroscience.

[48]  T. Hensch.  Critical period plasticity in local cortical circuits , 2005, Nature Reviews Neuroscience.

[49]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[50]  R. Malach,et al.  Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind , 2003, Nature Neuroscience.

[51]  F. Sengpiel,et al.  The Role of Activity in Development of the Visual System , 2002, Current Biology.

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

[53]  L. C. Katz,et al.  Development of cortical circuits: Lessons from ocular dominance columns , 2002, Nature Reviews Neuroscience.

[54]  David K. A. Barnes,et al.  correction: Early visual experience and face processing , 2001, Nature.

[55]  M. Stryker,et al.  The role of visual experience in the development of columns in cat visual cortex. , 1998, Science.

[56]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[57]  D. Hocking,et al.  An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[59]  K. L. Moore,et al.  The developing human , 1988 .

[60]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[61]  F. Y. Edgeworth.  On the Probable Errors of Frequency-Constants , 1908 .

[62]  Karl Pearson,et al.  Mathematical Contributions to the Theory of Evolution. IX. On the Principle of Homotyposis and Its Relation to Heredity, to the Variability of the Individual, and to that of the Race. Part I. Homotypos in the Vegetable Kingdom , 1901 .

[63]  K. Pearson,et al.  Mathematical contributions to the theory of evolution. IV. On the probable errors of frequency constants and on the influence of random selection on variation and correlation , 1898, Proceedings of the Royal Society of London.