Dyslexia and the magnocellular-parvocellular coactivaton hypothesis

Previous studies showed that the lateral masking of a fast-moving low spatial frequency (SF) target was strong when exerted by static flankers of lower or equal to the target SF and absent when flankers' SF was higher than the target's one. These masking and unmasking effects have been interpreted as due to Magnocellular-Magnocellular (M-M) inhibition and Parvocellular-on-Magnocellular (P-M) disinhibitory coactivation, respectively. Based on the hypothesis that the balance between the two systems is perturbed in Developmental Dyslexia (DD), we asked whether dyslexic children (DDs) behaved differently than Typically Developing children (TDs) in conditions of lateral masking. DDs and TDs performed a motion discrimination task, of a .5c/deg Gabor target moving at 16 deg/sec, either isolated or flanked by static Gabors with a SF of .125, .5 or 2 c/deg (Experiment 1). As a control, they also performed a contrast detection task of a static target, either isolated or flanked (Experiment 2). DDs did not perform any different from TDs with either a static target or an isolated moving target of low spatial frequency, thus suggesting efficient feedforward Magnocellular (M) and Parvocellular (P) processing. Also, DDs showed similar contrast thresholds to TDs in the M-M inhibition condition. Conversely, DDs did not recover from lateral masking in the M-P coactivation condition. In addition, their performance in this condition negatively correlated with non-words accuracy, supporting the suggestion that an inefficient Magno-Parvo coactivation may possibly be associated to both higher visual suppression and reduced perceptual stability during reading.

[1]  U. Polat,et al.  The architecture of perceptual spatial interactions , 1994, Vision Research.

[2]  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.

[3]  J. Stein,et al.  Visual motion sensitivity in dyslexia: evidence for temporal and energy integration deficits , 2000, Neuropsychologia.

[4]  T. Nealey,et al.  Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  James M. G. Tsui,et al.  Brief motion stimuli preferentially activate surround-suppressed neurons in macaque visual area MT , 2008, Current Biology.

[6]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[7]  D. Melcher,et al.  Investigating the role of temporal processing in developmental dyslexia: Evidence for a specific deficit in rapid visual segmentation , 2020, Psychonomic Bulletin & Review.

[8]  S. Leat,et al.  Development of Visual Acuity and Contrast Sensitivity in Children , 2009 .

[9]  Henry J. Alitto,et al.  Function of inhibition in visual cortical processing , 2010, Current Opinion in Neurobiology.

[10]  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.

[11]  Jan Churan,et al.  Interaction of spatial and temporal factors in psychophysical estimates of surround suppression. , 2009, Journal of vision.

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

[13]  A. Angelucci,et al.  Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. , 2006, Progress in brain research.

[14]  T. Lawton.  Improving Dorsal Stream Function in Dyslexics by Training Figure/Ground Motion Discrimination Improves Attention, Reading Fluency, and Working Memory , 2016, Front. Hum. Neurosci..

[15]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[16]  Marco Zorzi,et al.  Nested incremental modeling in the development of computational theories: the CDP+ model of reading aloud. , 2007, Psychological review.

[17]  M. Morgan,et al.  Observers can voluntarily shift their psychometric functions without losing sensitivity , 2011, Attention, Perception, & Psychophysics.

[18]  Gianluca Campana,et al.  Reducing Crowding by Weakening Inhibitory Lateral Interactions in the Periphery with Perceptual Learning , 2011, PloS one.

[19]  Keith D. White,et al.  Contrast sensitivity during saccadic eye movements , 1978, Vision Research.

[20]  H. Wimmer,et al.  A dual-route perspective on eye movements of dyslexic readers , 2010, Cognition.

[21]  C. Casco,et al.  Developmental dyslexia: A deficit in magnocellular-parvocellular co-activation, not simply in pure magnocellular activation , 2019, Vision Research.

[22]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[23]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

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

[25]  C. Distler,et al.  Attention and normalization circuits in macaque V1 , 2015, The European journal of neuroscience.

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

[27]  B. Skottun,et al.  Temporal Frequency and the Magnocellular and Parvocellular Systems , 2008 .

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

[29]  S. Gori,et al.  A different vision of dyslexia: Local precedence on global perception , 2017, Scientific Reports.

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

[31]  Michele Rucci,et al.  Contrast sensitivity reveals an oculomotor strategy for temporally encoding space , 2018, bioRxiv.

[32]  Simone Gori,et al.  Multiple Causal Links Between Magnocellular-Dorsal Pathway Deficit and Developmental Dyslexia. , 2016, Cerebral cortex.

[33]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[34]  B. Skottun,et al.  The Possible Relationship Between Visual Deficits and Dyslexia , 1999, Journal of learning disabilities.

[35]  M. Montague,et al.  The Proposed Changes for DSM-5 for SLD and ADHD , 2013, Journal of learning disabilities.

[36]  J. Stein.  The current status of the magnocellular theory of developmental dyslexia , 2019, Neuropsychologia.

[37]  David Burr,et al.  Suppression of the magnocellular pathway during saccades , 1996, Behavioural Brain Research.

[38]  B. Skottun,et al.  The magnocellular deficit theory of dyslexia: the evidence from contrast sensitivity , 2000, Vision Research.

[39]  E. Callaway,et al.  Parallel processing strategies of the primate visual system , 2009, Nature Reviews Neuroscience.

[40]  J. Shelley-Tremblay,et al.  Training on Movement Figure-Ground Discrimination Remediates Low-Level Visual Timing Deficits in the Dorsal Stream, Improving High-Level Cognitive Functioning, Including Attention, Reading Fluency, and Working Memory , 2017, Front. Hum. Neurosci..

[41]  C. Casco,et al.  Perceptual learning leads to long lasting visual improvement in patients with central vision loss. , 2016, Restorative neurology and neuroscience.

[42]  Nicola J. Pitchford,et al.  Encoding of rapid time-varying information is impaired in poor readers , 2017, Journal of vision.

[43]  P. Goolkasian,et al.  Letter identification and lateral masking in dyslexic and average readers. , 1990, The American journal of psychology.

[44]  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.

[45]  B Suresh Krishna,et al.  Surround Suppression Sharpens the Priority Map in the Lateral Intraparietal Area , 2022 .

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

[47]  Ignacio Serrano-Pedraza,et al.  Two Common Psychophysical Measures of Surround Suppression Reflect Independent Neuronal Mechanisms Task 1: Motion-direction Discrimination Task 2: Contrast Detection Suppression Index (si) , 2022 .

[48]  M Coltheart,et al.  DRC: a dual route cascaded model of visual word recognition and reading aloud. , 2001, Psychological review.

[49]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

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

[51]  C. Casco,et al.  Perceptual learning improves contrast sensitivity, visual acuity, and foveal crowding in amblyopia. , 2017, Restorative neurology and neuroscience.

[52]  Duje Tadin,et al.  Optimal size for perceiving motion decreases with contrast , 2005, Vision Research.

[53]  S. Gori,et al.  Is excessive visual crowding causally linked to developmental dyslexia? , 2019, Neuropsychologia.

[54]  D. Spinelli,et al.  Crowding, reading, and developmental dyslexia. , 2009, Journal of vision.

[55]  Marco Zorzi,et al.  The Development of Spelling-Sound Relationships in a Model of Phonological Reading , 1998 .

[56]  Duje Tadin,et al.  A Substantial and Unexpected Enhancement of Motion Perception in Autism , 2013, The Journal of Neuroscience.

[57]  H. Levitt.  Transformed up-down methods in psychoacoustics. , 1971, The Journal of the Acoustical Society of America.

[58]  J. Krystal,et al.  Impairment of GABAergic transmission in depression: new insights from neuroimaging studies. , 2000, Critical reviews in neurobiology.

[59]  E. Callaway,et al.  Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex , 1996, Nature.

[60]  A. Thiele,et al.  Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1 , 2008, The European journal of neuroscience.

[61]  Jong H. Yoon,et al.  GABA Concentration Is Reduced in Visual Cortex in Schizophrenia and Correlates with Orientation-Specific Surround Suppression , 2010, The Journal of Neuroscience.

[62]  M. Zorzi,et al.  Two routes or one in reading aloud? A connectionist dual-process model. , 1998 .

[63]  James L. McClelland,et al.  Understanding normal and impaired word reading: computational principles in quasi-regular domains. , 1996, Psychological review.

[64]  Randolph Blake,et al.  Perceptual consequences of centre–surround antagonism in visual motion processing , 2003, Nature.

[65]  Nicholas Shenker,et al.  Neurocognitive and Neuroplastic Mechanisms of Novel Clinical Signs in CRPS , 2016, Front. Hum. Neurosci..

[66]  Nicola J. Pitchford,et al.  Visual perception in dyslexia is limited by sub-optimal scale selection , 2017, Scientific Reports.

[67]  C. Casco,et al.  Suppressive effects on motion discrimination induced by transient flankers are reduced by perceptual learning. , 2015, Journal of vision.

[68]  D. Heeger,et al.  Brain activity in visual cortex predicts individual differences in reading performance. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[69]  A. Angelucci,et al.  Multiple components of surround modulation in primary visual cortex: Multiple neural circuits with multiple functions? , 2014, Vision Research.

[70]  C. Miniussi,et al.  Excitatory and inhibitory lateral interactions effects on contrast detection are modulated by tRNS , 2019, Scientific Reports.

[71]  M. Sigman,et al.  Opinion TRENDS in Cognitive Sciences Vol.9 No.7 July 2005 The neural code for written words: a proposal , 2022 .

[72]  Duje Tadin,et al.  Mechanisms of motion-based object segregation , 2014 .

[73]  L. P. O'Keefe,et al.  The influence of fixational eye movements on the response of neurons in area MT of the macaque , 1998, Visual Neuroscience.

[74]  T. Whitlock.  Dyslexia , 1989, The Lancet.

[75]  B. Skottun.  On the use of spatial frequency to isolate contributions from the magnocellular and parvocellular systems and the dorsal and ventral cortical streams , 2015, Neuroscience & Biobehavioral Reviews.