The similarity structure of distributed neural responses reveals the multiple representations of letters

NeuroImage

Volumn 89, Issue , 2014, Pages 331-344

  Rothlein, David ^a   Rapp, Brenda ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Abstract letter identity; Letter representation; Multivariate Pattern Analysis (MVPA); Reading and spelling networks; Representational Similarity Analysis (RSA); Visual Word Form Area (VWFA)

Indexed keywords

ADULT; ANALYTIC METHOD; ARTICLE; BOLD SIGNAL; CONTROLLED STUDY; DATA ANALYSIS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; LANGUAGE; LEFT HEMISPHERE; MALE; MOTOR PERFORMANCE; MULTIVARIATE PATTERN ANALYSIS REPRESENTATIONAL SIMILARITY ANALYSIS; NERVE CELL NETWORK; NERVE POTENTIAL; NEUROIMAGING; NORMAL HUMAN; PHONETICS; PRIORITY JOURNAL; READING; SPELLING; TEMPORAL LOBE; VISION; VISUAL STIMULATION;

ABSTRACT LETTER IDENTITY; LETTER REPRESENTATION; MULTIVARIATE PATTERN ANALYSIS (MVPA); READING AND SPELLING NETWORKS; REPRESENTATIONAL SIMILARITY ANALYSIS (RSA); VISUAL WORD FORM AREA (VWFA);

ADOLESCENT; ADULT; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; NERVE NET; READING; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84896698387     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.11.054     Document Type: Article

References (69)

1. Baker C.I., Liu J., Wald L.L., Kwong K.K., Benner T., Kanwisher N. Visual word processing and experiential origins of functional selectivity in human extrastriate cortex. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9087-9092.
2. Barsalou L.W. Grounded cognition. Annu. Rev. Psychol. 2008, 59:617-645.
3. Barton J.J.S., Fox C.J., Sekunova A., Iaria G. Encoding in the visual word form area: an fMRI adaptation study of words versus handwriting. J. Cogn. Neurosci. 2010, 22:1649-1661.
4. Barton J.J.S., Sekunova A., Sheldon C., Johnston S., Iaria G., Scheel M. Reading words, seeing style: the neuropsychology of word, font and handwriting perception. Neuropsychologia 2010, 48:3868-3877.
5. Bedny M., Caramazza A., Grossman E., Pascual-Leone A., Saxe R. Concepts are more than percepts: the case of action verbs. J. Neurosci. 2008, 28:11347-11353.
6. Besner D., Coltheart M., Davelaar E. Basic processes in reading: computation of abstract letter identities. Can. J. Psychol. 1984, 38:126-134.
7. Binder J.R., Medler D.A., Westbury C.F., Liebenthal E., Buchanan L. Tuning of the human left fusiform gyrus to sublexical orthographic structure. Neuroimage 2006, 33:739-748.
8. Boles D.B., Clifford J.E. An upper- and lowercase alphabetic similarity matrix, with derived generation similarity values. Behav. Res. Methods Instrum. Comput. 1989, 21:579-586.
9. Brunsdon R., Coltheart M., Nickels L. Severe developmental letter-processing impairment: a treatment case study. Cogn. Neuropsychol. 2006, 23:795-821.
10. Burgund E.D., Edwards J.K. Identity versus similarity priming for letters in left mid-fusiform cortex. Neuroreport 2008, 19:761-764.
11. Cohen L. Visual word recognition in the left and right hemispheres: anatomical and functional correlates of peripheral alexias. Cereb. Cortex 2003, 13:1313-1333.
12. Cohen L., Dehaene S., Naccache L., Lehéricy S., Dehaene-Lambertz G., Hénaff M.a., Michel F. The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. Brain 2000, 123:291-307.
13. Coltheart M. Disorders of reading and their implications for models of normal reading. Vis. Lang. 1981, 15:245-286.
14. Dehaene S., Cohen L. The unique role of the visual word form area in reading. Trends Cogn. Sci. 2011, 15:254-262.
15. Dehaene S., Naccache L., Cohen L., Bihan D.L., Mangin J.F., Poline J.B., Rivière D. Cerebral mechanisms of word masking and unconscious repetition priming. Nat. Neurosci. 2001, 4:752-758.
16. Dehaene S., Le Clec'H G., Poline J.-B., Le Bihan D., Cohen L. The visual word form area: a prelexical representation of visual words in the fusiform gyrus. Neuroreport 2002, 13:321-325.
17. Dehaene S., Jobert A., Naccache L., Ciuciu P., Poline J.-B., Le Bihan D., Cohen L. Letter binding and invariant recognition of masked words: behavioral and neuroimaging evidence. Psychol. Sci. 2004, 15:307-313.
18. Démonet J.-F., Taylor M.J., Chaix Y. Developmental dyslexia. Lancet 2004, 363:1451-1460.
19. Devlin J.T., Jamison H.L., Matthews P.M., Gonnerman L.M. Morphology and the internal structure of words. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:14984-14988.
20. Edelman S. Representation is representation of similarities. Behav. Brain Sci. 1998, 21:449-467. (discussion 467-98).
21. Gaillard R., Naccache L., Pinel P., Clémenceau S., Volle E., Hasboun D., Dupont S., Baulac M., Dehaene S., Adam C., et al. Direct intracranial, fMRI, and lesion evidence for the causal role of left inferotemporal cortex in reading. Neuron 2006, 50:191-204.
22. Gauthier I., Tarr M.J., Moylan J., Skudlarski P., Gore J.C., Anderson A.W. The fusiform "face area" is part of a network that processes faces at the individual level. J. Cogn. Neurosci. 2000, 12:495-504.
23. Glezer L.S., Jiang X., Riesenhuber M. Evidence for highly selective neuronal tuning to whole words in the "visual word form area". Neuron 2009, 62(2):199-204.
24. Grainger J., Rey A., Dufau S. Letter perception: from pixels to pandemonium. Trends Cogn. Sci. 2008, 12:381-387.
25. Grill-Spector K., Malach R. fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychol. (Amst) 2001, 107:293-321.
26. Hickok G. Eight problems for the mirror neuron theory of action understanding in monkeys and humans. J. Cogn. Neurosci. 2009, 21:1229-1243.
27. Hickok G., Poeppel D. The cortical organization of speech processing. Nat. Rev. Neurosci. 2007, 8:393-402.
28. Hull A.J. A letter-digit matrix of auditory confusions. Br. J. Psychol. 1973, 64:579-585.
29. Jackson N.E., Coltheart M. Routes to Reading Success and Failure: Towards and Integrated Cognitive Psychology of Atypical Reading 2001, Psychology Press, New York, NY. 1st ed.
30. James K.H., Atwood T.P. The role of sensorimotor learning in the perception of letter-like forms: tracking the causes of neural specialization for letters. Cogn. Neuropsychol. 2009, 26:91-110.
31. James K.H., Gauthier I. Letter processing automatically recruits a sensory-motor brain network. Neuropsychologia 2006, 44:2937-2949.
32. Jobard G., Crivello F., Tzourio-Mazoyer N. Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. Neuroimage 2003, 20:693-712.
33. Kinoshita S., Kaplan L. Priming of abstract letter identities in the letter match task. Q. J. Exp. Psychol. (Colchester) 2008, 61:1873-1885.
34. Kriegeskorte N. Pattern-information analysis: from stimulus decoding to computational-model testing. Neuroimage 2011, 56:411-421.
35. Kriegeskorte N., Goebel R., Bandettini P. Information-based functional brain mapping. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:3863-3868.
36. Kriegeskorte N., Mur M., Bandettini P. Representational similarity analysis-connecting the branches of systems neuroscience. Front. Syst. Neurosci. 2008, 2:1-28.
37. Kronbichler M., Klackl J., Richlan F., Schurz M., Staffen W., Ladurner G., Wimmer H. On the functional neuroanatomy of visual word processing: effects of case and letter deviance. J. Cogn. Neurosci. 2009, 21:222-229.
38. Longcamp M., Anton J.-L., Roth M., Velay J.-L. Visual presentation of single letters activates a premotor area involved in writing. Neuroimage 2003, 19:1492-1500.
39. Mahon B.Z., Caramazza A. A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content. J. Physiol. Paris 2008, 102:59-70.
40. Malach R., Reppas J.B., Benson R.R., Kwong K.K., Jiang H., Kennedy W.A., Ledden P.J., Brady T.J., Rosen B.R., Tootell R.B. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:8135-8139.
41. Miozzo M., Caramazza A. Varieties of pure alexia: the case of failure to access graphemic representations. Cogn. Neuropsychol. 1998, 15:203-238.
42. Nestor A., Behrmann M., Plaut D.C. The neural basis of visual word form processing: a multivariate investigation. Cereb. Cortex 2013, 23(7):1673-1684. (New York, N.Y. : 1991).
43. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
44. Paulesu E., McCrory E., Fazio F., Menoncello L., Brunswick N., Cappa S.F., Cotelli M., Cossu G., Corte F., Lorusso M., et al. A cultural effect on brain function. Nat. Neurosci. 2000, 3:91-96.
45. Plaut D.C., Behrmann M. Complementary neural representations for faces and words: a computational exploration. Cogn. Neuropsychol. 2011, 28:251-275.
46. Polk T.A., Farah M.J. Functional MRI evidence for an abstract, not perceptual, word-form area. J. Exp. Psychol. Gen. 2002, 131:65-72.
47. Price C.J., Devlin J.T. The myth of the visual word form area. Neuroimage 2003, 19:473-481.
48. Price C.J., Mummery C.J., Moore C.J., Frackowiak R.S.J., Friston K.J. Delineating necessary and sufficient neural systems with functional imaging studies of neuropsychological patients. J. Cogn. Neurosci. 1999, 11:371-382.
49. Pugh K.R., Mencl W.E., Jenner A.R., Katz L., Frost S.J., Lee J.R., Shaywitz S.E., Shaywitz B.a Neurobiological studies of reading and reading disability. J. Commun. Disord. 2001, 34:479-492.
50. Pulvermüller F. Brain mechanisms linking language and action. Nat. Rev. Neurosci. 2005, 6:576-582.
51. Purcell J.J., Napoliello E.M., Eden G.F. A combined fMRI study of typed spelling and reading. Neuroimage 2011, 55:750-762.
52. Purcell J.J., Turkeltaub P.E., Eden G.F., Rapp B. Examining the central and peripheral processes of written word production through meta-analysis. Front. Psychol. 2011, 2:1-16.
53. Qiao E., Vinckier F., Szwed M., Naccache L., Valabrègue R., Dehaene S., Cohen L. Unconsciously deciphering handwriting: subliminal invariance for handwritten words in the visual word form area. Neuroimage 2010, 49:1786-1799.
54. Raizada R.D.S., Kriegeskorte N. Pattern-information fMRI: New questions which it opens up and challenges which face it. Int. J. Imag. Syst. Tech. 2010, 20(1):31-41.
55. Rapcsak S.Z., Beeson P.M., Henry M.L., Leyden A., Kim E., Rising K., Andersen S., Cho H. Phonological dyslexia and dysgraphia: cognitive mechanisms and neural substrates. Cortex 2009, 45:575-591.
56. Rapp B., Caramazza A. From graphemes to abstract letter shapes: levels of representation in written spelling. J Exp. Psychol. Human 1997, 23(4):1130-1152.
57. Rapp B., Dufor O. The neurotopography of written word production: an fMRI investigation of the distribution of sensitivity to length and frequency. J. Cogn. Neurosci. 2011, 23:4067-4081.
58. Rapp B., Lipka K. The literate brain: the relationship between spelling and reading. J. Cogn. Neurosci. 2011, 23:1180-1197.
59. Rizzolatti G., Craighero L. The mirror-neuron system. Annu. Rev. Neurosci. 2004, 27:169-192.
60. Shaywitz B.A., Shaywitz S.E., Pugh K.R., Mencl W.E., Fulbright R.K., Skudlarski P., Constable R.T., Marchione K.E., Fletcher J.M., Lyon G.R., et al. Disruption of posterior brain systems for reading in children with developmental dyslexia. Biol. Psychiatry 2002, 52:101-110.
61. Shepard R.N., Chipman S. Second-order isomorphism of internal representations: shapes of states. Cogn. Psychol. 1970, 1:1-17.
62. Tenpenny P.L. Abstractionist versus episodic theories of repetition priming and word identification. Psychon. Bull. Rev. 1995, 2:339-363.
63. Tong F., Pratte M.S. Decoding patterns of human brain activity. Annu. Rev. Psychol. 2012, 63:483-509.
64. Tsapkini K., Rapp B. The orthography-specific functions of the left fusiform gyrus: evidence of modality and category specificity. Cortex 2010, 46:185-205.
65. Tsapkini K., Vindiola M., Rapp B. Patterns of brain reorganization subsequent to left fusiform damage: fMRI evidence from visual processing of words and pseudowords, faces and objects. Neuroimage 2011, 55:1357-1372.
66. Tulving E. Essentials of episodic memory 1983, (New York). O. U. Press (Ed.).
67. Turkeltaub P.E., Gareau L., Flowers D.L., Zeffiro T.A., Eden G.F. Development of neural mechanisms for reading. Nat. Neurosci. 2003, 6:767-773.
68. Vinckier F., Dehaene S., Jobert A., Dubus J.P., Sigman M., Cohen L. Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system. Neuron 2007, 55:143-156.
69. Wong A.C.-N., Jobard G., James K.H., James T.W., Gauthier I. Expertise with characters in alphabetic and nonalphabetic writing systems engage overlapping occipito-temporal areas. Cogn. Neuropsychol. 2009, 26:111-127.