Reliable individual-level neural markers of high-level language processing: A necessary precursor for relating neural variability to behavioral and genetic variability

NeuroImage

Volumn 139, Issue , 2016, Pages 74-93

  Mahowald, Kyle ^a   Fedorenko, Evelina ^b,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HMS   (United States)

Author keywords

Individual differences; Language system; Neural markers of language activity; Reliability

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN SIZE; CONTROLLED STUDY; EFFECT SIZE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GENETIC VARIABILITY; HEMISPHERIC DOMINANCE; HUMAN; HUMAN EXPERIMENT; LANGUAGE PROCESSING; MALE; NORMAL HUMAN; PRIORITY JOURNAL; RELIABILITY; TASK PERFORMANCE; ADOLESCENT; ANATOMY AND HISTOLOGY; BRAIN; BRAIN MAPPING; COGNITION; COMPREHENSION; COMPUTER ASSISTED DIAGNOSIS; LANGUAGE; MIDDLE AGED; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; ORGAN SIZE; PHYSIOLOGY; PROCEDURES; REFERENCE VALUE; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

BIOLOGICAL MARKER;

ADOLESCENT; ADULT; BIOMARKERS; BRAIN; BRAIN MAPPING; COGNITION; COMPREHENSION; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; LANGUAGE; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; ORGAN SIZE; REFERENCE VALUES; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

EID: 84975260905     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2016.05.073     Document Type: Article

References (81)

1. Amunts K., Lenzen M., Friederici A.D., Schleicher A., Morosan P., Palomero-Gallagher N., Zilles K. Broca's Region: Novel Organizational Principles and Multiple Receptor Mapping. PLoS Biol. 2010, 8(9):e1000489. 10.1371/journal.pbio.1000489.
2. Association, A.P., & others The Diagnostic and Statistical Manual of Mental Disorders: DSM 5. bookpointUS 2013.
3. Bavelier D., Corina D.P., Neville H.J. Brain and language: a perspective from sign language. Neuron 1998, 21(2):275-278.
4. Bedny M., Pascual-Leone A., Dodell-Feder D., Fedorenko E., Saxe R. Language processing in the occipital cortex of congenitally blind adults. Proc. Natl. Acad. Sci. 2011, 108:4429-4434. 10.1073/pnas.1014818108.
5. Belin P., Zatorre R.J., Lafaille P., Ahad P., Pike B. Voice-selective areas in human auditory cortex. Nature 2000, 403(6767):309-312.
6. Binder J.R., Frost J.A., Hammeke T.A., Cox R.W., Rao S.M., Prieto T. Human brain language areas identified by functional magnetic resonance imaging. J. Neurosci. 1997, 17(1):353-362.
7. Blank I.A., Kanwisher N., Fedorenko E. A functional dissociation between language and multiple-demand systems revealed in patterns of BOLD signal fluctuations. J. Neurophysiol. 2014, (jn-00884).
8. Carlson S.M., Moses L.J., Claxton L.J. Individual differences in executive functioning and theory of mind: an investigation of inhibitory control and planning ability. J. Exp. Child Psychol. 2004, 87(4):299-319.
9. Childers T.L., Houston M.J., Heckler S.E. Measurement of individual differences in visual versus verbal information processing. J. Consum. Res. 1985, 125-134.
10. Cohen M.S., DuBois R.M. Stability, repeatability, and the expression of signal magnitude in functional magnetic resonance imaging. J. Magn. Reson. Imaging: JMRI 1999, 10(1):33-40.
11. Colom R. Working memory is (almost) perfectly predicted by g. Intelligence 2004, 32(3):277-296. 10.1016/j.intell.2003.12.002.
12. Colombo J., Mitchell D.W., Coldren J.T., Freeseman L.J. Individual differences in infant visual attention: are short lookers faster processors or feature processors?. Child Dev. 1991, 62(6):1247-1257.
13. Conway A.R.A. Individual differences in working memory capacity: more evidence for a general capacity theory. Memory 1996, 4(6):577-590. 10.1080/741940997.
14. Cope N., Eicher J.D., Meng H., Gibson C.J., Hager K., Lacadie C., Gruen J.R. Variants in the DYX2 locus are associated with altered brain activation in reading-related brain regions in subjects with reading disability. NeuroImage 2012, 63(1):148-156. 10.1016/j.neuroimage.2012.06.037.
15. Daneman M., Carpenter P.A. Individual differences in working memory and reading. J. Verbal Learn. Verbal Behav. 1980, 19(4):450-466. 10.1016/S0022-5371(80)90312-6.
16. Diaz M.T., McCarthy G. A comparison of brain activity evoked by single content and function words: an fMRI investigation of implicit word processing. Brain Res. 2009, 1282:38-49. 10.1016/j.brainres.2009.05.043.
17. Dubois J., Adolphs R. Building a science of individual differences from fMRI. Trends Cogn. Sci. 2016, 20(6):425-443. (June). 10.1016/j.tics.2016.03.014.
18. Duncan J. The structure of cognition: attentional episodes in mind and brain. Neuron 2013, 80(1):35-50.
19. Duncan J., Seitz R.J., Kolodny J., Bor D., Herzog H., Ahmed A., Emslie H. A neural basis for general intelligence. Science 2000, 289(5478):457-460.
20. Fedorenko E. The role of domain-general cognitive control in language comprehension. Front. Psychol. 2014, 5. 10.3389/fpsyg.2014.00335.
21. Fedorenko E., Kanwisher N. Some regions within Broca's area do respond more strongly to sentences than to linguistically degraded stimuli: a comment on Rogalsky and Hickok (2011). J. Cogn. Neurosci. 2011, 23(10):2632-2635.
22. Fedorenko E., Thompson-Schill S.L. Reworking the language network. Trends Cogn. Sci. 2014, 18(3):120-126.
23. Fedorenko E., Hsieh P.-J., Nieto-Castanon A., Whitfield-Gabrieli S., Kanwisher N. New method for fMRI investigations of language: defining ROIs functionally in individual subjects. J. Neurophysiol. 2010, 104(2):1177-1194. 10.1152/jn.00032.2010.
24. Fedorenko E., Behr M.K., Kanwisher N. Functional specificity for high-level linguistic processing in the human brain. Proc. Natl. Acad. Sci. 2011, 108(39):16428-16433. 10.1073/pnas.1112937108.
25. Fedorenko E., Duncan J., Kanwisher N. Language-selective and domain-general regions lie side by side within Broca's area. Curr. Biol. 2012, 22(21):2059-2062.
26. Fedorenko E., McDermott J.H., Norman-Haignere S., Kanwisher N. Sensitivity to musical structure in the human brain. J. Neurophysiol. 2012, 108(12):3289-3300.
27. Fischl B., Rajendran N., Busa E., Augustinack J., Hinds O., Yeo B.T.T., Zilles K. Cortical folding patterns and predicting cytoarchitecture. Cereb. Cortex 2008, 18(8):1973-1980. 10.1093/cercor/bhm225.
28. Friedman L., Glover G.H., The FBIRN Consortium Reducing interscanner variability of activation in a multicenter fMRI study: controlling for signal-to-fluctuation-noise-ratio (SFNR) differences. NeuroImage 2006, 33(2):471-481. (November). 10.1016/j.neuroimage.2006.07.012.
29. Friedman L., Stern H., Brown G.G., Mathalon D.H., Turner J., Glover G.H., Gollub R.L., et al. Test-retest and between-site reliability in a multicenter fMRI study. Hum. Brain Mapp. 2008, 29(8):958-972. (August). 10.1002/hbm.20440.
30. Frost M.A., Goebel R. Measuring structural-functional correspondence: spatial variability of specialised brain regions after macro-anatomical alignment. NeuroImage 2012, 59(2):1369-1381. 10.1016/j.neuroimage.2011.08.035.
31. Gardner H., Hatch T. Educational implications of the theory of multiple intelligences. Educ. Res. 1989, 18(8):4-10. 10.3102/0013189X018008004.
32. Gernsbacher M.A. Cognitive processes and mechanisms in language comprehension: the structure building framework. Psychology of Learning and Motivation 1991, Vol. 27:217-263. Elsevier, (Retrieved from http://linkinghub.elsevier.com/retrieve/pii/S0079742108601255).
33. Gorgolewski K.J., Storkey A., Bastin M.E., Whittle I.R., Wardlaw J.M., Pernet C.R. A test-retest fMRI dataset for motor, language and spatial attention functions. GigaScience 2013, 2(1):6. 10.1186/2047-217X-2-6.
34. Grahn J.A., Schuit D. Individual differences in rhythmic ability: behavioral and neuroimaging investigations. Psychomusicology Music Mind Brain 2012, 22(2):105-121. 10.1037/a0031188.
35. Herrmann E., Call J., Hernandez-Lloreda M.V., Hare B., Tomasello M. Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science 2007, 317(5843):1360-1366. 10.1126/science.1146282.
36. Hinke R.M., Hu X., Stillman A.E., Kim S.-G., Merkle H., Salmi R., Ugurbil K. Functional magnetic resonance imaging of Broca's area during internal speech. NeuroReport 1993, 4(6):675-678. 10.1097/00001756-199306000-00018.
37. Hoogman M., Guadalupe T., Zwiers M.P., Klarenbeek P., Francks C., Fisher S.E. Assessing the effects of common variation in the FOXP2 gene on human brain structure. Front. Hum. Neurosci. 2014, 8. 10.3389/fnhum.2014.00473.
38. Insel T., Cuthbert B., Garvey M., Heinssen R., Pine D.S., Quinn K., Wang P. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatr. 2010, 167(7):748-751. 10.1176/appi.ajp.2010.09091379.
39. Julian J.B., Fedorenko E., Webster J., Kanwisher N. An algorithmic method for functionally defining regions of interest in the ventral visual pathway. NeuroImage 2012, 60(4):2357-2364. 10.1016/j.neuroimage.2012.02.055.
40. Just M.A., Carpenter P.A. A capacity theory of comprehension: individual differences in working memory. Psychol. Rev. 1992, 99(1):122-149. 10.1037/0033-295X.99.1.122.
41. Kane M.J., Engle R.W. The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: an individual-differences perspective. Psychon. Bull. Rev. 2002, 9(4):637-671.
42. Kanwisher N., McDermott J., Chun M.M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 1997, 17(11):4302.
43. Kriegeskorte N., Simmons W.K., Bellgowan P.S.F., Baker C.I. Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 2009, 12(5):535-540. 10.1038/nn.2303.
44. Krug A., Nieratschker V., Markov V., Krach S., Jansen A., Zerres K., Kircher T. Effect of CACNA1C rs1006737 on neural correlates of verbal fluency in healthy individuals. NeuroImage 2010, 49(2):1831-1836. 10.1016/j.neuroimage.2009.09.028.
45. Kuperberg G.R., Sitnikova T., Caplan D., Holcomb P.J. Electrophysiological distinctions in processing conceptual relationships within simple sentences. Cogn. Brain Res. 2003, 17(1):117-129. 10.1016/S0926-6410(03)00086-7.
46. Landi N., Frost S.J., Mencl W.E., Sandak R., Pugh K.R. Neurobiological bases of reading comprehension: insights from neuroimaging studies of word-level and text-level processing in skilled and impaired readers. Read. Writ. Q. 2013, 29(2):145-167. 10.1080/10573569.2013.758566.
47. Miller L.E., Saygin A.P. Individual differences in the perception of biological motion: links to social cognition and motor imagery. Cognition 2013, 128(2):140-148. 10.1016/j.cognition.2013.03.013.
48. Mischel W., Shoda Y., Rodriguez M.I. Delay of gratification in children. Science 1989, 244(4907):933-938.
49. Miyake A., Friedman N.P., Emerson M.J., Witzki A.H., Howerter A., Wager T.D. The unity and diversity of executive functions and their contributions to complex "frontal lobe" tasks: a latent variable analysis. Cogn. Psychol. 2000, 41(1):49-100.
50. Nieto-Castañón A., Fedorenko E. Subject-specific functional localizers increase sensitivity and functional resolution of multi-subject analyses. NeuroImage 2012, 63(3):1646-1669. 10.1016/j.neuroimage.2012.06.065.
51. Noppeney U., Price C.J. An fMRI study of syntactic adaptation. J. Cogn. Neurosci. 2004, 16(4):702-713. 10.1162/089892904323057399.
52. Ocklenburg S., Arning L., Gerding W.M., Epplen J.T., Güntürkün O., Beste C. Cholecystokinin A receptor (CCKAR) gene variation is associated with language lateralization. PLoS One 2013, 8(1):e53643. 10.1371/journal.pone.0053643.
53. Pakulak E., Neville H.J. Proficiency differences in syntactic processing of monolingual native speakers indexed by event-related potentials. J. Cogn. Neurosci. 2010, 22(12):2728-2744. 10.1162/jocn.2009.21393.
54. Perrachione T.K., Fedorenko E.G., Vinke L., Gibson E., Dilley L.C. Evidence for shared cognitive processing of pitch in music and language. PLoS One 2013, 8(8):e73372. 10.1371/journal.pone.0073372.
55. Petersen S., Fox P., Snyder A., Raichle M. Activation of extrastriate and frontal cortical areas by visual words and word-like stimuli. Science 1990, 249(4972):1041-1044. 10.1126/science.2396097.
56. Pinel P., Fauchereau F., Moreno A., Barbot A., Lathrop M., Zelenika D., Dehaene S. Genetic variants of FOXP2 and KIAA0319/TTRAP/THEM2 locus are associated with altered brain activation in distinct language-related regions. J. Neurosci. 2012, 32(3):817-825. 10.1523/JNEUROSCI.5996-10.2012.
57. Poppenk J., Evensmoen H.R., Moscovitch M., Nadel L. Long-axis specialization of the human hippocampus. Trends Cogn. Sci. 2013, 17(5):230-240. 10.1016/j.tics.2013.03.005.
58. Robertson D.A., Gernsbacher M.A., Guidotti S.J., Robertson R.R.W., Irwin W., Mock B.J., Campana M.E. Functional neuroanatomy of the cognitive process of mapping during discourse comprehension. Psychol. Sci. 2000, 11(3):255-260. 10.1111/1467-9280.00251.
59. Rombouts S.A., Barkhof F., Hoogenraad F.G., Sprenger M., Scheltens P. Within-subject reproducibility of visual activation patterns with functional magnetic resonance imaging using multislice echo planar imaging. Magn. Reson. Imaging 1998, 16(2):105-113.
60. Saxe R., Kanwisher N. People thinking about thinking people: the role of the temporo-parietal junction in "theory of mind. NeuroImage 2003, 19(4):1835-1842. 10.1016/S1053-8119(03)00230-1.
61. Scerri T.S., Morris A.P., Buckingham L.-L., Newbury D.F., Miller L.L., Monaco A.P., Paracchini S. DCDC2, KIAA0319 and CMIP are associated with reading-related traits. Biol. Psychiatry 2011, 70(3):237-245. 10.1016/j.biopsych.2011.02.005.
62. Scott, T. Gallée, J., and Fedorenko, E. A new fun and robust version of an fMRI localizer for the fronto-temporal language system, (in press).
63. Schoene-Bake J.-C., Keller S.S., Niehusmann P., Volmering E., Elger C., Deppe M., Weber B. In vivo mapping of hippocampal subfields in mesial temporal lobe epilepsy: relation to histopathology: hippocampal subfield mapping in mTLE. Hum. Brain Mapp. 2014, 35(9):4718-4728. 10.1002/hbm.22506.
64. Seghier M.L., Lazeyras F., Pegna A.J., Annoni J.-M., Khateb A. Group analysis and the subject factor in functional magnetic resonance imaging: analysis of fifty right-handed healthy subjects in a semantic language task. Hum. Brain Mapp. 2008, 29(4):461-477. 10.1002/hbm.20410.
65. Snijders T.M., Vosse T., Kempen G., Van Berkum J.J.A., Petersson K.M., Hagoort P. Retrieval and unification of syntactic structure in sentence comprehension: an fMRI study using word-category ambiguity. Cereb. Cortex 2009, 19(7):1493-1503. 10.1093/cercor/bhn187.
66. Spearman C. "General intelligence," objectively determined and measured. Am. J. Psychol. 1904, 15(2):201. 10.2307/1412107.
67. Spearman C. The Abilities of Man 1927.
68. Stein J.L., Medland S.E., Vasquez A.A., Hibar D.P., Senstad R.E., Winkler A.M., Thompson P.M. Identification of common variants associated with human hippocampal and intracranial volumes. Nat. Genet. 2012, 44(5):552-561. 10.1038/ng.2250.
69. Surprenant A.M., Watson C.S. Individual differences in the processing of speech and nonspeech sounds by normal-hearing listeners. J. Acoust. Soc. Am. 2001, 110(4):2085. 10.1121/1.1404973.
70. Suzuki R., Shimodaira H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 2006, 22(12):1540-1542.
71. Tahmasebi A.M., Davis M.H., Wild C.J., Rodd J.M., Hakyemez H., Abolmaesumi P., Johnsrude I.S. Is the link between anatomical structure and function equally strong at all cognitive levels of processing?. Cereb. Cortex 2012, 22(7):1593-1603. 10.1093/cercor/bhr205.
72. Team, R.C., & others R: A Language and Environment for Statistical Computing 2012.
73. Tie Y., Rigolo L., Norton I.H., Huang R.Y., Wu W., Orringer D., Golby A.J. Defining language networks from resting-state fMRI for surgical planning-a feasibility study: resting-state fMRI for language mapping. Hum. Brain Mapp. 2014, 35(3):1018-1030. 10.1002/hbm.22231.
74. Travis S.G., Huang Y., Fujiwara E., Radomski A., Olsen F., Carter R., Malykhin N.V. High field structural MRI reveals specific episodic memory correlates in the subfields of the hippocampus. Neuropsychologia 2014, 53:233-245. 10.1016/j.neuropsychologia.2013.11.016.
75. Traxler M.J., Johns C.L., Long D.L., Zirnstein M., Tooley K.M., Jonathan E. Individual differences in eye-movements during reading: working memory and speed-of-processing effects. J. Eye Mov. Res. 2012, 5(1):5.
76. Turken A.U., Dronkers N.F. The neural architecture of the language comprehension network: converging evidence from lesion and connectivity analyses. Front. Syst. Neurosci. 2011, 5. 10.3389/fnsys.2011.00001.
77. Vogel E.K., Machizawa M.G. Neural activity predicts individual differences in visual working memory capacity. Nature 2004, 428(6984):748-751.
78. Whalley H.C., O'Connell G., Sussmann J.E., Peel A., Stanfield A.C., Hayiou-Thomas M.E., Hall J. Genetic variation in CNTNAP2 alters brain function during linguistic processing in healthy individuals. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2011, 156(8):941-948. 10.1002/ajmg.b.31241.
79. Whitehouse A.J.O., Bishop D.V.M., Ang Q.W., Pennell C.E., Fisher S.E. CNTNAP2 variants affect early language development in the general population. Genes Brain Behav. 2011, 10(4):451-456. 10.1111/j.1601-183X.2011.00684.x.
80. Wilke M., Lidzba K. LI-tool: a new toolbox to assess lateralization in functional MR-data. J. Neurosci. Methods 2007, 163(1):128-136. 10.1016/j.jneumeth.2007.01.026.
81. Yue X., Nasr S., Devaney K.J., Holt D.J., Tootell R.B.H. FMRI analysis of contrast polarity in face-selective cortex in humans and monkeys. NeuroImage 2013, 76:57-69. 10.1016/j.neuroimage.2013.02.068.