Deficits in Magnocellular Pathway in Developmental Dyslexia: A Functional Magnetic Resonance Imaging-Electroencephalography Study

Abstract

Background: Magnocellular deficit theory is among the different hypotheses that have been proposed to explain the pathophysiology of developmental dyslexia (DD). Dysfunction of the magnocellular system in DD has been investigated using mainly visual evoked potentials (VEPs), particularly transient VEPs, although recently abnormal steady-state VEPs have also been reported. The brain regions responsible for the abnormal VEPs in DD have yet to be elucidated, however. In this study, we performed functional magnetic resonance imaging and electroencephalography (fMRI-EEG) simultaneously to elucidate the brain areas that were found in a previous study to be activated through stimulation of the magnocellular system, and then investigated the mechanism involved in the dysfunction seen in DD.Methods: Subjects were 20 healthy individuals (TYP group; 13 men, 7 women; mean ± standard deviation age, 26.3 ± 5.53 years) and 2 men with DD (aged 42 and 30 years). Images of brain activity were acquired with 3-Tesla MRI while the viewing the reversal of low-spatial frequency and low-contrast black-and-white sinusoidal gratings. EEG was recorded concurrently to obtain steady-state VEPs.Results: Stimulus frequency-dependent VEPs were observed in the posterior region of the brain in the TYP group; however, VEP amplitudes in both DD patients were clearly smaller than those in TYP. fMRI images revealed that both the primary and secondary visual cortices were activated by black-and- white sinusoidal gratings in the TYP group, whereas activity in the visual cortex overall was reduced in both DD patients.Conclusions: Present low spatial and high reversal frequency visual stimuli activated the primary visual cortex presumably through predominant activation of the magnocellular pathway. This finding indicates that some cases of adult patients of DD involve impairment of the visual magnocellular system.

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H. Yamamoto, Y. Kita, T. Kobayashi, H. Yamazaki, M. Kaga, H. Hoshino, T. Hanakawa, H. Yamamoto and M. Inagaki, "Deficits in Magnocellular Pathway in Developmental Dyslexia: A Functional Magnetic Resonance Imaging-Electroencephalography Study," Journal of Behavioral and Brain Science, Vol. 3 No. 2, 2013, pp. 168-178. doi: 10.4236/jbbs.2013.32017.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] WHO, “International Classification of Diseases (ICD 10),” 2009. http://www.who.int/classifications/icd/en/
[2] American Psychiatric Association, “Diagnostic and Statistical Manual of Mental Disorders,” 4th Edition, Washington DC, 2000.
[3] R. L. Peterson and B. F. Pennington, “Developmental Dyslexia,” Lancet, Vol. 379, No. 3830, 2012, pp. 1997-2007. doi:10.1016/S0140-6736(12)60198-6
[4] M. Inagaki, “Practical Guidelines for Diagnosis and Treatment in Patients with Specific Developmental Disorders [in Japan],” Shindan to Chiryousha, Tokyo, 2010.
[5] M. Livingstone and D. Hubel, “Segregation of Form, Color, Movement, and Depth: Anatomy, Physiology, and Perception,” Science, Vol. 240, No. 4853, 1988, pp. 740-749. doi:10.1126/science.3283936
[6] A. Galaburda and M. Livingstone, “Evidence for a Magnocellular Defect in Developmental Dyslexia,” Annals of the New York Academy of Sciences, Vol. 682, 1993, pp. 7082. doi:10.1111/j.1749-6632.1993.tb22960.x
[7] A. Romani, S. Conte, R. Callieco, R. Bergamaschi, M. Versino, G. Lanzi, C. A. Zambrino and V. Cosi, “Visual Evoked Potential Abnormalities in Dyslexia Children,” Functinal Neurology, Vol. 16, No. 3, 2001, pp. 219-229.
[8] Vaegan and F. C. Hollows, “Visual-Evoked Response, Pattern Electroretinogram, and Psychophysical Magnocellular Thresholds in Glaucoma, Optic Atrophy, and Dyslexia,” Optometry & Vision Science, Vol. 83, No. 7, pp. 486-498. doi:10.1097/01.opx.0000225920.97380.62
[9] S. Tobimatsu, “Transient and Steady-State VEPs-Reappraisal,” International Congress Series, Vol. 1232, 2002, pp. 207-211. doi:10.1016/S0531-5131(01)00840-8
[10] G. Bonmassar, D. P. Shwartz, A. K. Liu, K. K. Kwong, A. M. Dale and J. W. Belliveau, “Spatiotemporal Brain Imaging of Visual-Evoked Activity Using Interleaved EEG and fMRI Recordings,” Neuroimaging, Vol. 13, No. 6, 2001, pp. 1035-1043. doi:10.1006/nimg.2001.0754
[11] H. Tabuchi, T. Yokoyama, M. Shimogawara, K. Shiraki, E. Nagasaka and T. Miki, “Study of the Visual Evoked Magnetic Field with the M-Sequence Technique,” Visual Science, Vol. 43, No. 6, 2002, pp. 2045-2054.
[12] M. A. Pastor, J. Artieda, J. Arbizu, M. Valencia and J. C. Masdeu, “Human Cerebral Activation during SteadyState Visual-Evoked Responses,” Journal of Neuroscience, Vol. 23, No. 37, 2003, pp. 11621-11627.
[13] P. Krolak-Salmon, M. A. Henaff, C. Tallon-Baudry, B. Yvert, M. Guenot, A. Vighetto, F. Mauguiere and O. Bertrand, “Human Lateral Geniculate Nucleus and Visual Cortex Respond to Screen Flicker,” Annals of Neurology, Vol. 53, No. 1, 2003, pp. 73-80. doi:10.1002/ana.10403
[14] I. P. Fawcett, G. R. Barnes, A. Hillebrand and K. D. Singh, “The Temporal Frequency Tuning of Human Visual Cortex Investigated Using Synthetic Aperture Magnetometry,” Neuroimage, Vol. 21, No. 4, 2004, pp. 1542-1553. doi:10.1016/j.neuroimage.2003.10.045
[15] R. Srinivasan, E. Fornari, M. G. Knyazeva, R. Meuli and P. Maeder, “fMRI Responses in Medial Frontal Cortex That Depend on the Temporal Frequency of Visual Input,” Experimental Brain Research, Vol. 180, No. 4, 2007, pp. 677-691. doi:10.1007/s00221-007-0886-3
[16] F. Di Russo, S. Pitzalis, T. Aprile, G. Spitoni, F. Patria, A. Stella, D. Spinelli and S. A. Hillyard, “Spatiotemporal Analysis of the Cortical Sources of the Steady-State Visual Evoked Potential,” Human Brain Mapping, Vol. 28, No. 4, 2007, pp. 323-334. doi:10.1002/hbm.20276
[17] C. Porcaro, D. Ostwald and A. P. Bagshaw, “Functional Source Separation Improves the Quality of Single Trial Visual Evoked Potentials Recorded during Concurrent EEGfMRI,” Neuroimage, Vol. 50, No. 1, 2010, pp. 112-123. doi:10.1016/j.neuroimage.2009.12.002
[18] S. D. Mayhew, B. J. Macintosh, S. G. Dirckx, G. D. Iannetti and R. G. Wise, “Coupling of Simultaneously Acquired Electrophysiological and Haemodynamic Responses during Visual Stimulation,” Magn Reson Imaging, Vol. 28, No. 8, 2010, pp. 1066-1077. doi:10.1016/j.mri.2010.03.027
[19] Z. Liu, C. Rios, N. Zhang, L. Yang, W. Chen and B. He, “Linear and Nonlinear Relationships between Visual Stimuli, EEG and BOLD fMRI Signals,” Neuroimage, Vol. 50, No. 3, 2010, pp. 1054-1066.
[20] doi:10.1016/j.neuroimage.2010.01.017
[21] J. B. Demb, G. M. Boynton and D. J. Heeger, “Functional Magnetic Resonance Imaging of Early Visual Pathways in Dyslexia,” Journal of Neuroscience, Vol. 18, No. 17, 1998, pp. 6939-6951.
[22] G. F. Eden, J. W. VanMeter, J. M. Rumsey, J. M. Maisog, R. P. Woods and T. A. Zeffiro, “Abnormal Processing of Visual Motion in Dyslexia,” Nature, Vol. 382, No. 6586, 1996, pp. 66-69. doi:10.1038/382066a0
[23] T. Kobayashi, M. Inagaki, A. Gunji, K. Yatabe, Y. Kita, M. Kaga, T. Gotoh and T. Koike, “Developmental Changes of Rapid Automatized Naming and Hiragana Reading of Japanese Elementary School Children[in Japan],” No to Hattatsu, Vol. 43, No. 6, 2011, pp. 465-471.
[24] F. W. Campbell and L. Maffei, “Evidence for the Existence of Orientation and Size Detectors in the Human Visual System,” Journal of Physiology, Vol. 207, No. 3, 1970, pp. 635-652.
[25] H. Yamazaki, E. Adachi-Usami and J. Chiba, “Contrast Thresholds of Diabetic Patients Determined by VECP and Psychophysical Measurements,” Acta Opthalmology, Vol. 60, No. 3, 1982, pp. 386-392. doi:10.1111/j.1755-3768.1982.tb03029.x
[26] J. F. Schumacher, S. K. Thompson and C. A. Olman, “Contrast Response Functions for Single Gabor Patches: ROIBased Analysis Over-Represents Low-Contrast Patches for GE BOLD,” Front System of Neuroscience, Vol. 5, No. 19, 2011, pp. 1-10.
[27] G. T. Buracas and G. M. Boynton, “The Effect of Spatial Attention on Contrast Response Functions in Human Visual Cortex,” Journal of Neuroscience, Vol. 27, No. 1, 2007, pp. 93-97. doi:10.1523/JNEUROSCI.3162-06.2007
[28] F. D. Russo, D. Spinelli and M. C. Morrone, “Automatic Gain Control Contrast Mechanisms Are Modulated by Attention in Humans: Evidence from Visual Evoked Potentials,” Vision Research, Vol. 41, No. 19, 2001, pp. 2435-2447. doi:10.1016/S0042-6989(01)00134-1
[29] C. Boden and D. Giaschi, “M-Stream Deficits and ReadingRelated Visual Processes in Developmental Dyslexia,” Psychological Bullutin, Vol. 133, No. 2, 2007, pp. 346366. doi:10.1037/0033-2909.133.2.346
[30] J. M. Rumsey, B. Horwitz, B. C. Donohue, K. Nace, J. M. Maisog and P. Andreason, “Phonological and Orthographic Components of Word Recognition:A PET-rCBF Study,” Brain, Vol. 120, No. 5, 1997, pp. 739-759. doi:10.1093/brain/120.5.739
[31] J. M. Rumsey, K. Nace, B. Donohue, D. Wise, J. M. Maisog and P. Andreason, “A Positron Emission Tomographic Study of Impairedword Recognition and Phonological Processing in Dyslexic Men,” Archives of Neurology, Vol. 54, No. 5, 1997, pp. 562-573. doi:10.1001/archneur.1997.00550170042013

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