Morphological differences in the lateral geniculate nucleus associated with dyslexia
Mónica Giraldo-Chica, John P Hegarty 2nd, Keith A Schneider, Mónica Giraldo-Chica, John P Hegarty 2nd, Keith A Schneider
Abstract
Developmental dyslexia is a common learning disability characterized by normal intelligence but difficulty in skills associated with reading, writing and spelling. One of the most prominent, albeit controversial, theories of dyslexia is the magnocellular theory, which suggests that malfunction of the magnocellular system in the brain is responsible for the behavioral deficits. We sought to test the basis of this theory by directly measuring the lateral geniculate nucleus (LGN), the only location in the brain where the magnocellular and parvocellular streams are spatially disjoint. Using high-resolution proton-density weighted MRI scans, we precisely measured the anatomical boundaries of the LGN in 13 subjects with dyslexia (five female) and 13 controls (three female), all 22-26 years old. The left LGN was significantly smaller in volume in subjects with dyslexia and also differed in shape; no differences were observed in the right LGN. The functional significance of this asymmetry is unknown, but these results are consistent with the magnocellular theory and support theories of dyslexia that involve differences in the early visual system.
Keywords: Dyslexia; Lateral geniculate nucleus; Magnocellular; Parvocellular.
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References
- Amitay S., Ben-Yehudah G., Banai K., Ahissar M. Disabled readers suffer from visual and auditory impairments but not from a specific magnocellular deficit. Brain. 2002;125(10):2272–2285.
- Andrews T.J., Halpern S.D., Purves D. Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J. Neurosci. 1997;17(8):2859–2868. (PMID: )
- Avants B.B., Epstein C.L., Grossman M., Gee J.C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 2008;12(1):26–41.
- Carreiras M., Seghier M.L., Baquero S., Estévez A., Lozano A., Devlin J.T., Price C.J. An anatomical signature for literacy. Nature. 2009;461(7266):983–986.
- Dehaene S., Pegado F., Braga L.W., Ventura P., Nunes Filho G., Jobert A., Dehaene-Lambertz G., Kolinsky R., Morais J., Cohen L. How learning to read changes the cortical networks for vision and language. Science. 2010;330(6009):1359–1364.
- Demb J.B., Boynton G.M., Best M., Heeger D.J. Psychophysical evidence for a magnocellular pathway deficit in dyslexia. Vision Res. 1998;38(11):1555–1559.
- Demb J.B., Boynton G.M., Heeger D.J. Functional magnetic resonance imaging of early visual pathways in dyslexia. J. Neurosci. 1998;18(17):6939–6951. (PMID: )
- Démonet J.F., Taylor M.J., Chaix Y. Developmental dyslexia. Lancet. 2004;363(9419):1451–1460.
- Derrington A.M., Lennie P. Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J. Physiol. 1984;357:219–240.
- Eden G.F., Stein J.F., Wood H.M., Wood F.B. Temporal and spatial processing in reading disabled and normal children. Cortex. 1995;31(3):451–468.
- Eden G.F., Zeffiro T.A. Neural systems affected in developmental dyslexia revealed by functional neuroimaging. Neuron. 1998;21(2):279–282.
- Facoetti A., Paganoni P., Turatto M., Marzola V., Mascetti G.G. Visual–spatial attention in developmental dyslexia. Cortex. 2000;36(1):109–123.
- Facoetti A., Trussardi A.N., Ruffino M., Lorusso M.L., Cattaneo C., Galli R., Molteni M., Zorzi M. Multisensory spatial attention deficits are predictive of phonological decoding skills in developmental dyslexia. J. Cogn. Neurosci. 2010;22(5):1011–1025.
- Farrag A.F., Khedr E.M., Abel-Naser W. Impaired parvocellular pathway in dyslexic children. Eur. J. Neurol. 2002;9(4):359–363.
- Franceschini S., Gori S., Ruffino M., Pedrolli K., Facoetti A. A causal link between visual spatial attention and reading acquisition. Curr. Biol. 2012;22(9):814–819.
- Franceschini S., Gori S., Ruffino M., Viola S., Molteni M., Facoetti A. Action video games make dyslexic children read better. Curr. Biol. 2013;23(6):462–466.
- Gabrieli J.D. Dyslexia: a new synergy between education and cognitive neuroscience. Science. 2009;325(5938):280–283.
- Gabrieli J.D., Norton E.S. Reading abilities: importance of visual–spatial attention. Curr. Biol. 2012;22(9):R298–RR299.
- Galaburda A., Livingstone M. Evidence for a magnocellular defect in developmental dyslexia. Ann. N. Y. Acad. Sci. 1993;682:70–82.
- Gori S., Cecchini P., Bigoni A., Molteni M., Facoetti A. Magnocellular–dorsal pathway and sub-lexical route in developmental dyslexia. Front. Hum. Neurosci. 2014;8:460.
- Gori S., Facoetti A. Perceptual learning as a possible new approach for remediation and prevention of developmental dyslexia. Vision Res. 2014;99:78–87.
- Gori S., Mascheretti S., Giora E., Ronconi L., Ruffino M., Quadrelli E., Facoetti A., Marino C. The DCDC2 Intron 2 deletion impairs illusory motion perception unveiling the selective role of magnocellular–dorsal stream in reading (dis)ability. Cereb. Cortex. 2014
- Goswami U. Why theories about developmental dyslexia require developmental designs. Trends Cogn. Sci. 2003;7(12):534–540.
- Goswami U. A temporal sampling framework for developmental dyslexia. Trends Cogn. Sci. 2011;15(1):3–10.
- Hornickel J., Kraus N. Unstable representation of sound: a biological marker of dyslexia. J. Neurosci. 2013;33(8):3500–3504.
- Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17(2):825–841.
- Kevan A., Pammer K. Making the link between dorsal stream sensitivity and reading. Neuroreport. 2008;19(4):467–470.
- Kronbichler M., Hutzler F., Wimmer H. Dyslexia: verbal impairments in the absence of magnocellular impairments. Neuroreport. 2002;13(5):617–620.
- Laycock R., Crewther S.G. Towards an understanding of the role of the ‘magnocellular advantage’ in fluent reading. Neurosci. Biobehav. Rev. 2008;32(8):1494–1506.
- Lehongre K., Ramus F., Villiermet N., Schwartz D., Giraud A.L. Altered low-gamma sampling in auditory cortex accounts for the three main facets of dyslexia. Neuron. 2011;72(6):1080–1090.
- Livingstone M.S., Rosen G.D., Drislane F.W., Galaburda A.M. Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. Proc. Natl. Acad. Sci. U. S. A. 1991;88(18):7943–7947.
- Lovegrove W., Martin F., Bowling A., Blackwood M., Badcock D., Paxton S. Contrast sensitivity functions and specific reading disability. Neuropsychologia. 1982;20(3):309–315.
- Lovegrove W.J., Bowling A., Badcock D., Blackwood M. Specific reading disability: differences in contrast sensitivity as a function of spatial frequency. Science. 1980;210(4468):439–440.
- Martin F., Lovegrove W. The effects of field size and luminance on contrast sensitivity differences between specifically reading disabled and normal children. Neuropsychologia. 1984;22(1):73–77.
- Martin F., Lovegrove W. Flicker contrast sensitivity in normal and specifically disabled readers. Perception. 1987;16(2):215–221.
- Mason A.J., Cornelissen P.L., Fowler M.S., Stein J.F. Static and flicker contrast sensitivity in children with unstable visual direction sense. Clin. Vis. Sci. 1993;8:345–353.
- McLean G.M., Stuart G.W., Coltheart V., Castles A. Visual temporal processing in dyslexia and the magnocellular deficit theory: the need for speed? J. Exp. Psychol. Hum. Percept. Perform. 2011;37(6):1957–1975.
- Merigan W.H., Maunsell J.H. How parallel are the primate visual pathways? Annu. Rev. Neurosci. 1993;16:369–402.
- O'Connor D.H., Fukui M.M., Pinsk M.A., Kastner S. Attention modulates responses in the human lateral geniculate nucleus. Nat. Neurosci. 2002;5(11):1203–1209.
- Okubo M., Nicholls M.E. Hemispheric asymmetry in temporal resolution: contribution of the magnocellular pathway. Psychon. Bull. Rev. 2005;12(4):755–759.
- Olulade O.A., Napoliello E.M., Eden G.F. Abnormal visual motion processing is not a cause of dyslexia. Neuron. 2013;79:180–190.
- Pammer K. Temporal sampling in vision and the implications for dyslexia. Front. Hum. Neurosci. 2013;7:933.
- Peterson R.L., Pennington B.F. Developmental dyslexia. Lancet. 2012;379(9830):1997–2007.
- Ramus F. Neurobiology of dyslexia: a reinterpretation of the data. Trends Neurosci. 2004;27(12):720–726.
- Ruffino M., Gori S., Boccardi D., Molteni M., Facoetti A. Spatial and temporal attention in developmental dyslexia. Front. Hum. Neurosci. 2014;8:331.
- Ruffino M., Trussardi A.N., Gori S., Finzi A., Giovagnoli S., Menghini D., Benassi M., Molteni M., Bolzani R., Vicari S., Facoetti A. Attentional engagement deficits in dyslexic children. Neuropsychologia. 2010;48(13):3793–3801.
- Satz P., Rardin D., Ross J. An evaluation of a theory of specific developmental dyslexia. Child Dev. 1971;42(6):2009–2021.
- Schneider K.A. Subcortical mechanisms of feature-based attention. J. Neurosci. 2011;31(23):8643–8653.
- Schneider K.A., Kastner S. Effects of sustained spatial attention in the human lateral geniculate nucleus and superior colliculus. J. Neurosci. 2009;29(6):1784–1795.
- Schwarzkopf D.S., Rees G. Subjective size perception depends on central visual cortical magnification in human v1. PLOS ONE. 2013;8(3):e60550.
- Schwarzkopf D.S., Song C., Rees G. The surface area of human V1 predicts the subjective experience of object size. Nat. Neurosci. 2011;14(1):28–30.
- Shaywitz S.E. Dyslexia. N. Engl. J. Med. 1998;338(5):307–312.
- Skottun B.C. On the use of metacontrast to assess magnocellular function in dyslexic readers. Percept. Psychophys. 2001;63(7):1271–1274.
- Skottun B.C. On the use of the Ternus test to assess magnocellular function. Perception. 2001;30(12):1449–1457.
- Skottun B.C. On the use of red stimuli to isolate magnocellular responses in psychophysical experiments: a perspective. Vis. Neurosci. 2004;21(1):63–68.
- Skottun B.C., Skoyles J. Yellow filters, magnocellular responses, and reading. Int. J. Neurosci. 2007;117(2):287–293.
- Skottun B.C., Skoyles J.R. Is coherent motion an appropriate test for magnocellular sensitivity? Brain Cogn. 2006;61(2):172–180.
- Skottun B.C., Skoyles J.R. The use of phantom contours to isolate magnocellular and parvocellular responses. Int. J. Neurosci. 2006;116(3):315–320.
- Smith S.M., Nichols T.E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2009;44(1):83–98.
- Solan H.A., Hansen P.C., Shelley-Tremblay J., Ficarra A. Coherent motion threshold measurements for M-cell deficit differ for above- and below-average readers. Optometry. 2003;74(11):727–734. (PMID: )
- Solan H.A., Shelley-Tremblay J.F., Hansen P.C., Larson S. Is there a common linkage among reading comprehension, visual attention, and magnocellular processing? J. Learn. Disabil. 2007;40(3):270–278.
- Solomon S.G., Peirce J.W., Dhruv N.T., Lennie P. Profound contrast adaptation early in the visual pathway. Neuron. 2004;42(1):155–162.
- Sperling A.J., Lu Z.L., Manis F.R., Seidenberg M.S. Deficits in perceptual noise exclusion in developmental dyslexia. Nat. Neurosci. 2005;8(7):862–863.
- Sperling A.J., Lu Z.L., Manis F.R., Seidenberg M.S. Motion-perception deficits and reading impairment: it's the noise, not the motion. Psychol. Sci. 2006;17(12):1047–1053.
- Stein J. The magnocellular theory of developmental dyslexia. Dyslexia. 2001;7(1):12–36.
- Stein J. Dyslexia: the role of vision and visual Attention. Curr Dev Disord Rep. 2014;1(4):267–280.
- Stein J., Talcott J., Walsh V. Controversy about the visual magnocellular deficit in developmental dyslexics. Trends Cogn. Sci. 2000;4(6):209–211.
- Stein J., Walsh V. To see but not to read; the magnocellular theory of dyslexia. Trends Neurosci. 1997;20(4):147–152.
- Stein J.F. Developmental dyslexia, neural timing and hemispheric lateralisation. Int. J. Psychophysiol. 1994;18(3):241–249.
- Steinman S.B., Steinman B.A., Garzia R.P. Vision and attention. II: is visual attention a mechanism through which a deficient magnocellular pathway might cause reading disability? Optom. Vis. Sci. 1998;75(9):674–681.
- Swan D., Goswami U. Phonological awareness deficits in developmental dyslexia and the phonological representations hypothesis. J. Exp. Child Psychol. 1997;66(1):18–41.
- Tallal P. Auditory temporal perception, phonics, and reading disabilities in children. Brain Lang. 1980;9(2):182–198.
- Valdois S., Lassus-Sangosse D., Lobier M. Impaired letter-string processing in developmental dyslexia: what visual-to-phonology code mapping disorder? Dyslexia. 2012;18(2):77–93.
- van Herten M., Pasman J., van Leeuwen T.H., Been P.H., van der Leij A., Zwarts F., Maassen B. Differences in AERP responses and atypical hemispheric specialization in 17-month-old children at risk of dyslexia. Brain Res. 2008;1201:100–105.
- Vanni S., Uusitalo M.A., Kiesilä P., Hari R. Visual motion activates V5 in dyslexics. Neuroreport. 1997;8(8):1939–1942.
- Verghese A., Kolbe S.C., Anderson A.J., Egan G.F., Vidyasagar T.R. Functional size of human visual area V1: a neural correlate of top-down attention. Neuroimage. 2014;93(1):47–52.
- Victor J.D., Conte M.M., Burton L., Nass R.D. Visual evoked potentials in dyslexics and normals: failure to find a difference in transient or steady-state responses. Vis. Neurosci. 1993;10(5):939–946.
- Vidyasagar T.R. Neural underpinnings of dyslexia as a disorder of visuo-spatial attention. Clin. Exp. Optom. 2004;87(1):4–10.
- Vidyasagar T.R. Reading into neuronal oscillations in the visual system: implications for developmental dyslexia. Front. Hum. Neurosci. 2013;7:811.
- Vidyasagar T.R., Pammer K. Impaired visual search in dyslexia relates to the role of the magnocellular pathway in attention. Neuroreport. 1999;10(6):1283–1287.
- Vidyasagar T.R., Pammer K. Dyslexia: a deficit in visuo-spatial attention, not in phonological processing. Trends Cogn. Sci. 2010;14(2):57–63.
- Wagner R.K., Torgesen J.K., Rashotte C.A. Comprehensive Test of Phonological Processing. Pro-Ed; Austin, TX: 1999.
- Wechsler D. Wechsler Adult Intelligence Scale. third edition. Pearson; San Antonio, TX.: 1997.
- Wilmer J.B., Richardson A.J., Chen Y., Stein J.F. Two visual motion processing deficits in developmental dyslexia associated with different reading skills deficits. J. Cogn. Neurosci. 2004;16(4):528–540.
- Woodcock R.W., McGrew K.S., Mather N. Woodcock–Johnson III Tests of Achievement. Riverside Publications; Rolling Meadows, IL: 2001. 2007.
- Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation–maximization algorithm. I. E.E.E. Transactions Med. Imaging. 2001;20(1):45–57.
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