Multiple Causal Links Between Magnocellular-Dorsal Pathway Deficit and Developmental Dyslexia.

Although impaired auditory-phonological processing is the most popular explanation of developmental dyslexia (DD), the literature shows that the combination of several causes rather than a single factor contributes to DD. Functioning of the visual magnocellular-dorsal (MD) pathway, which plays a key role in motion perception, is a much debated, but heavily suspected factor contributing to DD. Here, we employ a comprehensive approach that incorporates all the accepted methods required to test the relationship between the MD pathway dysfunction and DD. The results of 4 experiments show that (1) Motion perception is impaired in children with dyslexia in comparison both with age-match and with reading-level controls; (2) pre-reading visual motion perception-independently from auditory-phonological skill-predicts future reading development, and (3) targeted MD trainings-not involving any auditory-phonological stimulation-leads to improved reading skill in children and adults with DD. Our findings demonstrate, for the first time, a causal relationship between MD deficits and DD, virtually closing a 30-year long debate. Since MD dysfunction can be diagnosed much earlier than reading and language disorders, our findings pave the way for low resource-intensive, early prevention programs that could drastically reduce the incidence of DD.

[1]  Guinevere F. Eden,et al.  Neural Systems Affected in Developmental Dyslexia Revealed by Functional Neuroimaging , 1998, Neuron.

[2]  Steven R. Holloway,et al.  Perceptual Learning of Motion Leads to Faster Flicker Perception , 2006, PloS one.

[3]  Simone Gori,et al.  The DCDC2 intron 2 deletion impairs illusory motion perception unveiling the selective role of magnocellular-dorsal stream in reading (dis)ability. , 2015, Cerebral cortex.

[4]  M. Snowling From language to reading and dyslexia. , 2001, Dyslexia.

[5]  Trichur Raman Vidyasagar,et al.  Dyslexia: a deficit in visuo-spatial attention, not in phonological processing , 2010, Trends in Cognitive Sciences.

[6]  J. Stein Visual Contributions to Reading Difficulties: The Magnocellular Theory , 2012 .

[7]  Kai Hamburger,et al.  Last but not least. , 2007, Perception.

[8]  Caroline Witton,et al.  On the relationship between dynamic visual and auditory processing and literacy skills; results from a large primary-school study. , 2002, Dyslexia.

[9]  J. Ziegler,et al.  Extra-large letter spacing improves reading in dyslexia , 2012, Proceedings of the National Academy of Sciences.

[10]  E. Valenza,et al.  The attentional 'zoom-lens' in 8-month-old infants. , 2016, Developmental science.

[11]  K. Pammer,et al.  Symbol-string sensitivity and adult performance in lexical decision , 2005, Brain and Language.

[12]  Catherine Boden,et al.  Children with dyslexia: evidence for visual attention deficits in perception of rapid sequences of objects , 2004, Vision Research.

[13]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  S. Dehaene,et al.  How Learning to Read Changes the Cortical Networks for Vision and Language , 2010, Science.

[15]  Patrizio Emanuele Tressoldi,et al.  DDE-2,Batteria per la valutazione della dislessia e della disortografia evolutiva-2. , 2007 .

[16]  R. Klein,et al.  The evidence for a temporal processing deficit linked to dyslexia: A review , 1995, Psychonomic bulletin & review.

[17]  A. Facoetti,et al.  Different underlying neurocognitive deficits in developmental dyslexia: A comparative study , 2010, Neuropsychologia.

[18]  L. Chelazzi,et al.  Sluggish engagement and disengagement of non-spatial attention in dyslexic children , 2008, Cortex.

[19]  Miguel Torres,et al.  Cancer predisposition: Searching for early events , 2015, Nature Reviews Cancer.

[20]  V. Walsh Dyslexia: Reading between the laminae , 1995, Current Biology.

[21]  J. Ziegler,et al.  Reading acquisition, developmental dyslexia, and skilled reading across languages: a psycholinguistic grain size theory. , 2005, Psychological bulletin.

[22]  U. Goswami,et al.  Amplitude envelope onsets and developmental dyslexia: A new hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Coltheart,et al.  Is there a causal link from phonological awareness to success in learning to read? , 2004, Cognition.

[24]  H. Wimmer,et al.  Functional abnormalities in the dyslexic brain: A quantitative meta‐analysis of neuroimaging studies , 2009, Human brain mapping.

[25]  H. Renvall,et al.  Impaired processing of rapid stimulus sequences in dyslexia , 2001, Trends in Cognitive Sciences.

[26]  P. Skudlarski,et al.  Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention , 2004, Biological Psychiatry.

[27]  M. Coltheart,et al.  The visual magnocellular-dorsal dysfunction in Chinese children with developmental dyslexia impedes Chinese character recognition , 2014, Scientific Reports.

[28]  S. Gori,et al.  Spatial and temporal attention in developmental dyslexia , 2014, Front. Hum. Neurosci..

[29]  K. Pammer,et al.  Attentional shifting and the role of the dorsal pathway in visual word recognition , 2006, Neuropsychologia.

[30]  Mark S. Seidenberg,et al.  Cognitive Development: Gaming Your Way Out of Dyslexia? , 2013, Current Biology.

[31]  M. Beran,et al.  Do rhesus monkeys (Macaca mulatta) perceive illusory motion? , 2015, Animal Cognition.

[32]  S. Scott,et al.  Intact But Less Accessible Phonetic Representations in Adults with Dyslexia , 2013, Science.

[33]  R. Woods,et al.  Abnormal processing of visual motion in dyslexia revealed by functional brain imaging , 1996, Nature.

[34]  N. Kraus,et al.  Unstable Representation of Sound: A Biological Marker of Dyslexia , 2013, The Journal of Neuroscience.

[35]  D. Giaschi,et al.  M-stream deficits and reading-related visual processes in developmental dyslexia. , 2007, Psychological bulletin.

[36]  J. Stinissen WPPSI, Wechsler Preschool and Primary Scale of Intelligence , 1981 .

[37]  Simone Gori,et al.  The neural basis of the Enigma illusion: A transcranial magnetic stimulation study , 2011, Neuropsychologia.

[38]  A. Facoetti Spatial Attention Disorders in Developmental Dyslexia: Towards the Prevention of Reading Acquisition Deficits , 2012 .

[39]  Elizabeth S Norton,et al.  Neurobiology of dyslexia , 2014, Current Opinion in Neurobiology.

[40]  S. Gori,et al.  Perceptual learning as a possible new approach for remediation and prevention of developmental dyslexia , 2014, Vision Research.

[41]  F. Martin,et al.  A theoretical and experimental case for a visual deficit in specific reading disability , 1986 .

[42]  Simone Gori,et al.  A new motion illusion based on competition between two kinds of motion processing units: The Accordion Grating , 2011, Neural Networks.

[43]  Régine Kolinsky,et al.  Illiterate to literate: behavioural and cerebral changes induced by reading acquisition , 2015, Nature Reviews Neuroscience.

[44]  Andrea Facoetti,et al.  The DCDC2/intron 2 deletion and white matter disorganization: Focus on developmental dyslexia , 2014, Cortex.

[45]  Marco Dadda,et al.  Do Fish Perceive Illusory Motion? , 2014, Scientific Reports.

[46]  Zhong-Lin Lu,et al.  Motion-Perception Deficits and Reading Impairment , 2006, Psychological science.

[47]  G. Mangun,et al.  Developmental dyslexia: Passive visual stimulation provides no evidence for a magnocellular processing defect , 1996, Neuropsychologia.

[48]  D. Basso,et al.  TMS on right frontal eye fields induces an inflexible focus of attention. , 2014, Cerebral cortex.

[49]  D. H. Kelly Frequency Doubling in Visual Responses , 1966 .

[50]  J. Stein,et al.  Contrast sensitivity and coherent motion detection measured at photopic luminance levels in dyslexics and controls , 1995, Vision Research.

[51]  U. Goswami Sensory theories of developmental dyslexia: three challenges for research , 2014, Nature Reviews Neuroscience.

[52]  Usha Goswami,et al.  Why theories about developmental dyslexia require developmental designs , 2003, Trends in Cognitive Sciences.

[53]  A. Toga,et al.  Neuroanatomical precursors of dyslexia identified from pre-reading through to age 11. , 2014, Brain : a journal of neurology.

[54]  J. Stein,et al.  To see but not to read; the magnocellular theory of dyslexia , 1997, Trends in Neurosciences.

[55]  Trichur Raman Vidyasagar A neuronal model of attentional spotlight: parietal guiding the temporal , 1999, Brain Research Reviews.

[56]  Aaron R. Seitz,et al.  Changing expectations about speed alters perceived motion direction , 2011, Current Biology.

[57]  Andrea Facoetti,et al.  Visual attentional engagement deficits in children with Specific Language Impairment and their role in real-time language processing , 2013, Cortex.

[58]  K. Pammer,et al.  Predicting early reading skills from pre-reading measures of dorsal stream functioning , 2009, Neuropsychologia.

[59]  Aaron R. Seitz,et al.  What a difference a parameter makes: A psychophysical comparison of random dot motion algorithms , 2009, Vision Research.

[60]  Simone Gori,et al.  Decreased Coherent Motion Discrimination in Autism Spectrum Disorder: The Role of Attentional Zoom-Out Deficit , 2012, PloS one.

[61]  Eileen M. Napoliello,et al.  Abnormal Visual Motion Processing Is Not a Cause of Dyslexia , 2013, Neuron.

[62]  E. Giora,et al.  The perceptual expansion of a filled area depends on textural characteristics , 2010, Vision Research.

[63]  Alexandre Pouget,et al.  Improved Probabilistic Inference as a General Learning Mechanism with Action Video Games , 2010, Current Biology.

[64]  D. Badcock,et al.  Specific reading disability: differences in contrast sensitivity as a function of spatial frequency. , 1980, Science.

[65]  S. Gori,et al.  How the visual aspects can be crucial in reading acquisition? The intriguing case of crowding and developmental dyslexia. , 2015, Journal of vision.

[66]  Aaron R. Seitz,et al.  The phenomenon of task-irrelevant perceptual learning , 2009, Vision Research.

[67]  J. Fletcher,et al.  Specific reading disability (dyslexia): what have we learned in the past four decades? , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[68]  S. Donnadieu,et al.  Visual attentional blink in dyslexic children: Parameterizing the deficit , 2010, Vision Research.

[69]  G. Geiger,et al.  Wide and Diffuse Perceptual Modes Characterize Dyslexics in Vision and Audition , 2008, Perception.

[70]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[71]  M. Molteni,et al.  Pleiotropic Effects of DCDC2 and DYX1C1 Genes on Language and Mathematics Traits in Nuclear Families of Developmental Dyslexia , 2011, Behavior genetics.

[72]  John F. Stein,et al.  Impaired neuronal timing in developmental dyslexia—the magnocellular hypothesis , 1999 .

[73]  R. Goebel,et al.  Reduced Neural Integration of Letters and Speech Sounds Links Phonological and Reading Deficits in Adult Dyslexia , 2009, Current Biology.

[74]  P. Bryant,et al.  Categorizing sounds and learning to read—a causal connection , 1983, Nature.

[75]  B. Pennington From single to multiple deficit models of developmental disorders , 2006, Cognition.

[76]  M. Zorzi,et al.  Visual spatial attention and speech segmentation are both impaired in preschoolers at familial risk for developmental dyslexia. , 2010, Dyslexia.

[77]  M. Nobile,et al.  The role of DCDC2 genetic variants and low socioeconomic status in vulnerability to attention problems , 2015, European Child & Adolescent Psychiatry.

[78]  Trichur Raman Vidyasagar Reading into neuronal oscillations in the visual system: implications for developmental dyslexia , 2013, Front. Hum. Neurosci..

[79]  DH Hubel,et al.  Psychophysical evidence for separate channels for the perception of form, color, movement, and depth , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[80]  M. Livingstone,et al.  Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[81]  S. Gori,et al.  Attentional engagement deficits in dyslexic children , 2010, Neuropsychologia.

[82]  S. Gori,et al.  A Causal Link between Visual Spatial Attention and Reading Acquisition , 2012, Current Biology.

[83]  Andrea Facoetti,et al.  Multisensory Spatial Attention Deficits Are Predictive of Phonological Decoding Skills in Developmental Dyslexia , 2010, Journal of Cognitive Neuroscience.

[84]  J. Gabrieli Dyslexia: A New Synergy Between Education and Cognitive Neuroscience , 2009, Science.

[85]  Emily A. Farris,et al.  White Matter Morphometric Changes Uniquely Predict Children’s Reading Acquisition , 2014, Psychological science.

[86]  S. Gori,et al.  Action Video Games Make Dyslexic Children Read Better , 2013, Current Biology.

[87]  J. Hegarty,et al.  Morphological differences in the lateral geniculate nucleus associated with dyslexia , 2015, NeuroImage: Clinical.

[88]  Aaron R. Seitz,et al.  Unattended exposure to components of speech sounds yields same benefits as explicit auditory training , 2010, Cognition.

[89]  L. Spillmann,et al.  Detection vs. grouping thresholds for elements differing in spacing, size and luminance. An alternative approach towards the psychophysics of Gestalten , 2010, Vision Research.

[90]  Psychologie Wechsler Preschool and Primary Scale of Intelligence , 2011, Definitions.

[91]  I. Mattingly Speech cues and sign stimuli. , 1972, American scientist.

[92]  S. Valdois,et al.  Developmental dyslexia: The visual attention span deficit hypothesis , 2007, Cognition.

[93]  R. Shapley,et al.  The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[94]  J. Stein Dyslexia: the Role of Vision and Visual Attention , 2014, Current Developmental Disorders Reports.

[95]  J. Stein,et al.  Probing the neurocognitive trajectories of children’s reading skills , 2013, Neuropsychologia.

[96]  Haiying Meng,et al.  DCDC2 genetic variants and susceptibility to developmental dyslexia , 2012, Psychiatric genetics.

[97]  P. Tallal Improving language and literacy is a matter of time , 2004, Nature Reviews Neuroscience.

[98]  Simone Gori,et al.  Perceptual Compromise between Apparent and Veridical Motion Indices: The Unchained-Dots Illusion , 2010, Perception.

[99]  C Witton,et al.  Dynamic sensory sensitivity and children's word decoding skills. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[100]  A. Rees,et al.  Sensitivity to dynamic auditory and visual stimuli predicts nonword reading ability in both dyslexic and normal readers , 1998, Current Biology.

[101]  Mary M. Conte,et al.  Visual evoked potentials in dyslexics and normals: Failure to find a difference in transient or steady-state responses , 1993, Visual Neuroscience.

[102]  J. Wouters,et al.  Coherent motion sensitivity and reading development in the transition from prereading to reading stage. , 2011, Child development.

[103]  Simone Gori,et al.  The Riddle of the Rotating-Tilted-Lines Illusion , 2008, Perception.

[104]  A. Galaburda,et al.  Evidence for a Magnocellular Defect in Developmental Dyslexia a , 1993, Annals of the New York Academy of Sciences.

[105]  E. Giora,et al.  Deeper attentional masking by lateral objects in children with autism , 2013, Brain and Cognition.

[106]  B. Pennington,et al.  Developmental dyslexia , 2012, The Lancet.

[107]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[108]  F. Richlan Developmental dyslexia: dysfunction of a left hemisphere reading network , 2012, Front. Hum. Neurosci..

[109]  Stanislas Dehaene,et al.  Reading normal and degraded words: Contribution of the dorsal and ventral visual pathways , 2008, NeuroImage.

[110]  P. Cecchini,et al.  Magnocellular-dorsal pathway and sub-lexical route in developmental dyslexia , 2014, Front. Hum. Neurosci..

[111]  Simone Gori,et al.  A New Motion Illusion: The Rotating-Tilted-Lines Illusion , 2006, Perception.

[112]  K. Pammer,et al.  Symbol-string sensitivity and children’s reading , 2004, Brain and Language.

[113]  J. Stein What is Developmental Dyslexia? , 2018, Brain sciences.

[114]  Neil W. Roach,et al.  Impaired filtering of behaviourally irrelevant visual information in dyslexia. , 2007, Brain : a journal of neurology.

[115]  Kristen Pammer,et al.  Visual deficits in pre-readers at familial risk for dyslexia , 2008, Vision Research.

[116]  D. Burr,et al.  A cortical area that responds specifically to optic flow, revealed by fMRI , 2000, Nature Neuroscience.

[117]  E. Giora,et al.  Perceptual multistability in figure-ground segregation using motion stimuli. , 2008, Acta psychologica.

[118]  P. Tallal Language disabilities in children: a perceptual or linguistic deficit? , 1980, Journal of pediatric psychology.

[119]  P. Skudlarski,et al.  DCDC2 is associated with reading disability and modulates neuronal development in the brain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[120]  J. Stein,et al.  The magnocellular theory of developmental dyslexia. , 2001, Dyslexia.

[121]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[122]  M. Morrone,et al.  Strong Motion Deficits in Dyslexia Associated with DCDC2 Gene Alteration , 2015, The Journal of Neuroscience.

[123]  Simone Gori,et al.  The novelty of the "Accordion Grating Illusion" , 2013, Neural Networks.

[124]  A. Bureau,et al.  An assessment of gene‐by‐environment interactions in developmental dyslexia‐related phenotypes , 2012, Genes, brain, and behavior.

[125]  G. Schulte-Körne,et al.  Clinical neurophysiology of visual and auditory processing in dyslexia: A review , 2010, Clinical Neurophysiology.

[126]  Geoffrey W. Stuart,et al.  Contrast sensitivity in subgroups of developmental dyslexia , 2003, Vision Research.

[127]  Mark S. Seidenberg,et al.  Deficits in perceptual noise exclusion in developmental dyslexia , 2005, Nature Neuroscience.

[128]  J. Rabe-Jabłońska,et al.  [Affective disorders in the fourth edition of the classification of mental disorders prepared by the American Psychiatric Association -- diagnostic and statistical manual of mental disorders]. , 1993, Psychiatria polska.

[129]  T R Vidyasagar,et al.  Gating of neuronal responses in macaque primary visual cortex by an attentional spotlight , 1998, Neuroreport.

[130]  K. Stanovich,et al.  Early reading acquisition and its relation to reading experience and ability 10 years later. , 1997, Developmental psychology.

[131]  Merav Ahissar,et al.  Disabled readers suffer from visual and auditory impairments but not from a specific magnocellular deficit. , 2002, Brain : a journal of neurology.

[132]  Aaron R. Seitz,et al.  Psychophysics: Is subliminal learning really passive? , 2003, Nature.

[133]  S. Crewther,et al.  Towards an understanding of the role of the ‘magnocellular advantage’ in fluent reading , 2008, Neuroscience & Biobehavioral Reviews.

[134]  Guinevere F. Eden,et al.  An Investigation into the Origin of Anatomical Differences in Dyslexia , 2014, The Journal of Neuroscience.

[135]  Simone Gori,et al.  Zoom-out attentional impairment in children with autism spectrum disorder , 2013, Cortex.

[136]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[137]  Simone Gori,et al.  Mathematical analysis of the Accordion Grating illusion: A differential geometry approach to introduce the 3D aperture problem , 2011, Neural Networks.

[138]  Stanislas Dehaene,et al.  Learning to read improves the structure of the arcuate fasciculus. , 2014, Cerebral cortex.