Impaired auditory sampling in dyslexia: Further evidence from combined fMRI and EEG

Frontiers in Human Neuroscience

Volumn , Issue JUL, 2013, Pages

  Lehongre, Katia ^a   Morillon, Benjamin ^b   Giraud, Anne Lise ^c   Ramus, Franck ^d  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b NewYork Presbyterian Hospital   (United States)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d PSL RESEARCH UNIVERSITY   (France)

Author keywords

Auditory sampling; Delta oscillation; Dyslexia; EEG fMRI; Gamma oscillation; Phonemic processing; Theta oscillation

Indexed keywords

ADULT; ARTICLE; AUDIOVISUAL EQUIPMENT; AUDITORY CORTEX; BRAIN DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DELTA RHYTHM; DEVELOPMENTAL DISORDER; DYSLEXIA; ELECTROENCEPHALOGRAPHY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAMMA RHYTHM; HEMISPHERIC DOMINANCE; HUMAN; LEFT HEMISPHERE; MALE; OSCILLATION; RIGHT HEMISPHERE; SAMPLING; THETA RHYTHM;

EID: 84933673621     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00454     Document Type: Article

References (58)

1. Abrams, D.A., Nicol, T., Zecker, S., and Kraus, N. (2008). Right-hemisphere auditory cortex is dominant for coding syllable patterns in speech. J Neurosci 28, 3958-3965.
2. Abrams, D.A., Nicol, T., Zecker, S., and Kraus, N. (2009). Abnormal cortical processing of the syllable rate of speech in poor readers. J Neurosci 29, 7686-7693.
3. Adlard, A., and Hazan, V. (1998). Speech perception in children with specific reading difficulties (dyslexia). Q J Exp Psychol A 51, 153-177.
4. Altarelli, I., Leroy, F., Dehaene-Lambertz, G., and Ramus, F. (submitted). Planum temporale asymmetry in developmental dyslexia: revisiting an old question.
5. Altarelli, I., Monzalvo, K., lannuzzi, S., Fluss, J., Billard, C., Ramus, F., and Dehaene-Lambertz, G. (in press). A functionally guided approach to the morphometry of occipito-temporal regions in developmental dyslexia: evidence for differential effects in boys and girls. Journal of Neuroscience.
6. Babiloni, C., Stella, G., Buffo, P., Vecchio, F., Onorati, P., Muratori, C., Miano, S., Gheller, F., Antonaci, L., Albertini, G., and Rossini, P.M. (2012). Cortical sources of resting state EEG rhythms are abnormal in dyslexic children. Clinical Neurophysiology 123, 2384-2391.
7. Brett, M., Anton, J.-L., Valabregue, R., and Poline, P. (2002). "Region of interest analysis using an SPM toolbox " ', in: 8th International Conference on Functional Mapping of the Human Brain. (Sendai, Japan).
8. Darki, F., Peyrard-Janvid, M., Matsson, H., Kere, J., and Klingberg, T. (2012). Three Dyslexia Susceptibility Genes, DYX1C1, DCDC2, and KIAA0319, Affect Temporo-Parietal White Matter Structure. Biol Psychiatry 72, 671-676.
9. Dunn, L.M., Thériault, C.M., and Dunn, L.M. (1993). Echelle de vocabulaire en images Peabody (EVIP). Toronto:Psycan.
10. Eckert, M. (2004). Neuroanatomical markers for dyslexia: a review of dyslexia structural imaging studies. Neuroscientist 10, 362-371.
11. Evans, T.M., Flowers, D.L., Napoliello, E.M., and Eden, G.F. (2013). Sex-specific gray matter volume differences in females with developmental dyslexia. Brain Struct Funct.
12. Frederickson, N., Frith, U., and Reason, R. (1997). Phonological Assessment Battery. Windsor, UK:: nferNelson.
13. Galaburda, A.M., Corsiglia, J., Rosen, G.D., and Sherman, G.F. (1987). Planum temporale asymmetry: Reappraisal since Geschwind and Levitsky. Neuropsychologia 25, 853-868.
14. Galaburda, A.M., Sherman, G.F., Rosen, G.D., Aboitiz, F., and Geschwind, N. (1985). Developmental dyslexia: four consecutive patients with cortical anomalies. Ann Neurol 18, 222-233.
15. Giraud, A.L., Kleinschmidt, A., Poeppel, D., Lund, T.E., Frackowiak, R.S., and Laufs, H. (2007). Endogenous cortical rhythms determine cerebral specialization for speech perception and production. Neuron 56, 1127-1134.
16. Giraud, A.L., and Poeppel, D. (2012). Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci 15, 511-517.
17. Giraud, A.L., and Ramus, F. (2013). Neurogenetics and auditory processing in developmental dyslexia. Curr Opin Neurobiol 23, 37-42.
18. Goswami, U. (2011). A temporal sampling framework for developmental dyslexia. Trends Cogn Sci 15, 310.
19. Goswami, U., Gerson, D., and Astruc, L. (2010). Amplitude envelope perception, phonology and prosodic sensitivity in children with developmental dyslexia. Reading and Writing 23, 995-1019.
20. Goswami, U., Wang, H.L.S., Cruz, A., Fosker, T., Mead, N., and Huss, M. (2011). Language-universal Sensory Deficits in Developmental Dyslexia: English, Spanish, and Chinese. Journal of Cognitive Neuroscience 23, 325-337.
21. Hamalainen, J.A., Rupp, A., Soltesz, F., Szucs, D., and Goswami, U. (2012). Reduced phase locking to slow amplitude modulation in adults with dyslexia: an MEG study. Neuroimage 59, 2952-2961.
22. Han, J., Mody, M., and Ahlfors, S.P. (2012). Gamma phase locking modulated by phonological contrast during auditory comprehension in reading disability. NeuroReport 23, 851-856 810.1097/WNR.1090b1013e32835818e32835811.
23. Heim, S., Friedman, J.T., Keil, A., and Benasich, A.A. (2011). Reduced sensory oscillatory activity during rapid auditory processing as a correlate of language-learning impairment. Journal of Neurolinguistics 24, 538-555.
24. Herrmann, C.S., and Debener, S. (2008). Simultaneous recording of EEG and BOLD responses: a historical perspective. Int J Psychophysiol 67, 161-168.
25. Howard, M.F., and Poeppel, D. (2012). The neuromagnetic response to spoken sentences: co-modulation of theta band amplitude and phase. NeuroImage 60, 2118-2127.
26. Humphreys, P., Kaufmann, W.E., and Galaburda, A.M. (1990). Developmental dyslexia in women: neuropathological findings in three patients. Ann Neurol 28, 727-738.
27. Laufs, H. (2012). A personalized history of EEG-fMRI integration. NeuroImage 62, 1056-1067.
28. Laufs, H., Krakow, K., Sterzer, P., Eger, E., Beyerle, A., Salek-Haddadi, A., and Kleinschmidt, A. (2003). Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest. Proc Natl Acad Sci U S A 100, 11053-11058.
29. Lee, J.H., Durand, R., Gradinaru, V., Zhang, F., Goshen, I., Kim, D.S., Fenno, L.E., Ramakrishnan, C., and Deisseroth, K. (2010). Global and local fMRI signals driven by neurons defined optogenetically by type and wiring. Nature 465, 788-792.
30. Lefavrais, P. (1967). Test de l'Alouette, Second Edition Paris: Editions du Centre de Psychologie Appliquée.
31. Lehongre, K., Ramus, F., Villiermet, N., Schwartz, D., and Giraud, A.L. (2011). Altered low-gamma sampling in auditory cortex accounts for the three main facets of dyslexia. Neuron 72, 10801090.
32. Lindgren, S.D., De Renzi, E., and Richman, L.C. (1985). Cross-national comparisons of developmental dyslexia in Italy and the United States. Child Development 56, 1404-1417.
33. Linkersdorfer, J., Lonnemann, J., Lindberg, S., Hasselhorn, M., and Fiebach, C.J. (2012). Grey matter alterations co-localize with functional abnormalities in developmental dyslexia: an ALE metaanalysis. PLoS One 7, e43122.
34. Logothetis, N.K. (2010). Bold claims for optogenetics. Nature 468, E3-4; discussion E4-5.
35. Magri, C., Schridde, U., Murayama, Y., Panzeri, S., and Logothetis, N.K. (2012). The amplitude and timing of the BOLD signal reflects the relationship between local field potential power at different frequencies. J Neurosci 32, 1395-1407.
36. Mandelkow, H., Halder, P., Boesiger, P., and Brandeis, D. (2006). Synchronization facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth. NeuroImage 32, 1120-1126.
37. Mody, M., Studdert-Kennedy, M., and Brady, S. (1997). Speech perception deficits in poor readers: auditory processing or phonological coding? J Exp Child Psychol 64, 199-231.
38. Morillon, B., Lehongre, K., Frackowiak, R.S.J., Ducorps, A., Kleinschmidt, A., Poeppel, D., and Giraud, A.L. (2010). Neurophysiological origin of human brain asymmetry for speech and language. Proceedings of the National Academy of Sciences of the United States of America 107, 1868818693.
39. Oostenveld, R., Fries, P., Maris, E., and Schoffelen, J.M. (2011). FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011, 156869.
40. Pennington, B.F. (2006). From single to multiple deficit models of developmental disorders. Cognition 101, 385-413.
41. Pinel, P., Fauchereau, F., Moreno, A., Barbot, A., Lathrop, M., Zelenika, D., Le Bihan, D., Poline, J.B., Bourgeron, T., and Dehaene, S. (2012). Genetic Variants of FOXP2 and KIAA0319/TTRAP/THEM2 Locus Are Associated with Altered Brain Activation in Distinct Language-Related Regions. Journal of Neuroscience 32, 817-825.
42. Poelmans, H., Luts, H., Vandermosten, M., Boets, B., Ghesquiere, P., and Wouters, J. (2012). Auditory steady state cortical responses indicate deviant phonemic-rate processing in adults with dyslexia. Ear Hear 33, 134-143.
43. Poeppel, D. (2003). The analysis of speech in different temporal integration windows: cerebral lateralization as 'asymmetric sampling in time'. Speech Communication 41, 245-255.
44. Ramus, F., and Ahissar, M. (2012). Developmental dyslexia: the difficulties of interpreting poor performance, and the importance of normal performance. Cognitive Neuropsychology 29, 104122.
45. Ramus, F., and Szenkovits, G. (2008). What phonological deficit? Quarterly Journal of Experimental Psychology 61, 129-141.
46. Raven, J., Raven, J.C., and Court, J.H. (1998). Advanced Progressive Matrices. Oxford, UK: Oxford Psychologists Press.
47. Richardson, F.M., and Price, C.J. (2009). Structural MRI studies of language function in the undamaged brain. Brain Struct Funct 213, 511-523.
48. Richlan, F., Kronbichler, M., and Wimmer, H. (2011). Meta-analyzing brain dysfunctions in dyslexic children and adults. NeuroImage 56, 1735-1742.
49. Rosa, M.J., Daunizeau, J., and Friston, K.J. (2010a). EEG-fMRI integration: a critical review of biophysical modeling and data analysis approaches. J Integr Neurosci 9, 453-476.
50. Rosa, M.J., Kilner, J., Blankenburg, F., Josephs, O., and Penny, W. (2010b). Estimating the transfer function from neuronal activity to BOLD using simultaneous EEG-fMRI. NeuroImage 49, 14961509.
51. Serniclaes, W., Van Heghe, S., Mousty, P., Carre, R., and Sprenger-Charolles, L. (2004). Allophonic mode of speech perception in dyslexia. J Exp Child Psychol 87, 336-361.
52. Soroli, E., Szenkovits, G., and Ramus, F. (2010). Exploring dyslexics' phonological deficit III: foreign speech perception and production. Dyslexia 16, 318-340.
53. Tallal, P. (1980). Auditory temporal perception, phonics, and reading disabilities in children. Brain and Language 9, 182-198.
54. Telkemeyer, S., Rossi, S., Koch, S.P., Nierhaus, T., Steinbrink, J., Poeppel, D., Obrig, H., and Wartenburger, I. (2009). Sensitivity of newborn auditory cortex to the temporal structure of sounds. J Neurosci 29, 14726-14733.
55. Vellutino, F.R., Fletcher, J.M., Snowling, M.J., and Scanlon, D.M. (2004). Specific reading disability (dyslexia): what have we learned in the past four decades? J Child Psychol & Psychiat 45, 2-40.
56. Wagner, R.K., and Torgesen, J.K. (1987). The nature of phonological processing and its causal role in the acquisition of reading skills. Psychological Bulletin 101, 192-212.
57. Wechsler, D. (2000). WAIS-III: Echelle de l'intelligence de Wechsler pour adultes. Troisième Edition. Paris: Editions du Centre de Psychologie Appliquée.
58. World Health Organization (2011). International Statistical Classification of Diseases and Related Health Problems-10th revision. Geneva: World Health Organization.