Neural organization of spoken language revealed by lesion-symptom mapping

Nature Communications

Volumn 6, Issue , 2015, Pages

  Mirman, Daniel ^a,b   Chen, Qi ^a,c   Zhang, Yongsheng ^d   Wang, Ze ^d,e   Faseyitan, Olufunsho K ^d   Coslett, H Branch ^a,d   Schwartz, Myrna F ^a  

^a MOSS REHABILITATION RESEARCH INSTITUTE   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c SOUTH CHINA NORMAL UNIVERSITY   (China)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e HANGZHOU NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ASSESSMENT METHOD; BRAIN; LANGUAGE; MAPPING METHOD; NEUROLOGY; TECHNOLOGICAL CHANGE;

ADULT; AGED; ARTICLE; BRAIN DAMAGE; BRAIN MAPPING; COGNITION; COMPUTER ASSISTED TOMOGRAPHY; FEMALE; FRONTAL CORTEX; HUMAN; LANGUAGE DISABILITY; LANGUAGE TEST; LINGUISTICS; MAJOR CLINICAL STUDY; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITOFRONTAL FASCICULUS; PREMOTOR CORTEX; RECOGNITION; SPEECH; SPEECH DISCRIMINATION; SUPERIOR TEMPORAL GYRUS; SUPRAMARGINAL GYRUS; TEMPORAL LOBE; TRACTOGRAPHY; UNCINATE FASCICULUS; WERNICKE AREA; WHITE MATTER; ANOMIA; APHASIA; APHASIA, BROCA; APHASIA, CONDUCTION; BRAIN; CEREBROVASCULAR ACCIDENT; COMPLICATION; FRONTAL LOBE; MIDDLE AGED; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY; SEMANTICS; SPEECH PERCEPTION;

SYLVIA;

ADULT; AGED; ANOMIA; APHASIA; APHASIA, BROCA; APHASIA, CONDUCTION; BRAIN; BRAIN MAPPING; FEMALE; FRONTAL LOBE; HUMANS; MALE; MIDDLE AGED; NEURAL PATHWAYS; NEUROIMAGING; RECOGNITION (PSYCHOLOGY); SEMANTICS; SPEECH; SPEECH PERCEPTION; STROKE; TEMPORAL LOBE; WHITE MATTER;

EID: 84928007832     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7762     Document Type: Article

References (70)

1. Lichtheim, L. On aphasia. Brain 7, 433-484 (1885).
2. Geschwind, N. The organization of language and the brain. Science 170, 940-944 (1970).
3. Poeppel, D. & Hickok, G. S. Towards a new functional anatomy of language. Cognition 92, 1-12 (2004).
4. Patterson, K. & Lambon Ralph, M. A. Selective disorders of reading? Curr. Opin. Neurobiol. 9, 235-239 (1999).
5. Menenti, L., Gierhan, S. M. E., Segaert, K. & Hagoort, P. Shared language: Overlap and segregation of the neuronal infrastructure for speaking and listening revealed by functional MRI. Psychol. Sci. 22, 1173-1182 (2011).
6. Hickok, G. S. & Poeppel, D. The cortical organization of speech processing. Nat. Rev. Neurosci. 8, 393-402 (2007).
7. Hickok, G. S. & Poeppel, D. Dorsal and ventral streams: A framework for understanding aspects of the functional anatomy of language. Cognition 92, 67-99 (2004).
8. Rauschecker, J. P. & Scott, S. K. Maps and streams in the auditory cortex: Nonhuman primates illuminate human speech processing. Nat. Neurosci. 12, 718-724 (2009).
9. Binder, J. R. & Desai, R. H. The neurobiology of semantic memory. Trends Cogn. Sci. 15, 527-536 (2011).
10. Patterson, K. E., Nestor, P. J. & Rogers, T. T. Where do you know what you know? The representation of semantic knowledge in the human brain. Nat. Rev. Neurosci. 8, 976-987 (2007).
11. Damasio, H., Tranel, D., Grabowski, T., Adolphs, R. & Damasio, A. R. Neural systems behind word and concept retrieval. Cognition 92, 179-229 (2004).
12. Dronkers, N. F., Wilkins, D. P., Van Valin, R. D., Redfern, B. B. & Jaeger, J. J. Lesion analysis of the brain areas involved in language comprehension. Cognition 92, 145-177 (2004).
13. Catani, M. & Mesulam, M.-M. The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state. Cortex 44, 953-961 (2008).
14. Catani, M. & Ffytche, D. H. The rises and falls of disconnection syndromes. Brain 128, 2224-2239 (2005).
15. Mirman, D. et al. A large, searchable, web-based database of aphasic performance on picture naming and other tests of cognitive function. Cogn. Neuropsychol. 27, 495-504 (2010).
16. Bates, E. et al. Voxel-based lesion-symptom mapping. Nat. Neurosci. 6, 448-450 (2003).
17. Schwartz, M. F. et al. Anterior temporal involvement in semantic word retrieval: Voxel-based lesion-symptom mapping evidence from aphasia. Brain 132, 3411-3427 (2009).
18. Walker, G. M. et al. Support for anterior temporal involvement in semantic error production in aphasia: New evidence from VLSM. Brain Lang. 117, 110-122 (2011).
19. Mesulam, M.-M. et al. Neurology of anomia in the semantic variant of primary progressive aphasia. Brain 132, 2553-2565 (2009).
20. Mesulam, M.-M. et al. Words and objects at the tip of the left temporal lobe in primary progressive aphasia. Brain 136, 601-618 (2013).
21. Martin, A. The representation of object concepts in the brain. Annu. Rev. Psychol. 58, 25-45 (2007).
22. Visser, M., Jefferies, E. & Lambon Ralph, M. A. Semantic processing in the anterior temporal lobes: A meta-analysis of the functional neuroimaging literature. J. Cogn. Neurosci. 22, 1083-1094 (2010).
23. Guo, C. C. et al. Anterior temporal lobe degeneration produces widespread network-driven dysfunction. Brain 136, 2979-2991 (2013).
24. Seghier, M. L. The angular gyrus: Multiple functions and multiple subdivisions. Neuroscientist 19, 43-61 (2013).
25. Catani, M. & De Schotten, M. T. Atlas of Human Brain Connections 519 (Oxford University Press, 2012).
26. Rilling, J. K. et al. The evolution of the arcuate fasciculus revealed with comparative DTI. Nat. Neurosci. 11, 426-428 (2008).
27. Mori, S., Wakana, S., Zijl van, P. C. M. & Nagae-Poetscher, L. M. MRI Atlas of Human White Matter 276 (Elsevier, 2005).
28. Han, Z. et al. White matter structural connectivity underlying semantic processing: Evidence from brain damaged patients. Brain 136, 2952-2965 (2013).
29. Kümmerer, D. et al. Damage to ventral and dorsal language pathways in acute aphasia. Brain 136, 619-629 (2013).
30. Moritz-Gasser, S., Herbet, G. & Duffau, H. Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: A brain electrostimulation study. Neuropsychologia 51, 1814-1822 (2013).
31. Buchsbaum, B. R. et al. Conduction aphasia, sensory-motor integration, and phonological short-term memory-an aggregate analysis of lesion and fMRI data. Brain Lang. 119, 119-128 (2011).
32. Schwartz, M. F., Faseyitan, O., Kim, J. & Coslett, H. B. The dorsal stream contribution to phonological retrieval in object naming. Brain 135, 3799-3814 (2012).
33. Fridriksson, J. et al. Impaired speech repetition and left parietal lobe damage. J. Neurosci. 30, 11057-11061 (2010).
34. Dell, G. S., Schwartz, M. F., Nozari, N., Faseyitan, O. & Coslett, H. B. Voxelbased lesion-parameter mapping: Identifying the neural correlates of a computational model of word production. Cognition 128, 380-396 (2013).
35. DeWitt, I. & Rauschecker, J. P. Phoneme and word recognition in the auditory ventral stream. Proc. Natl Acad. Sci. USA 109, E505-E514 (2012).
36. Gow, D. W. The cortical organization of lexical knowledge: A dual lexicon model of spoken language processing. Brain Lang. 121, 273-288 (2012).
37. Caramazza, A. & Hillis, A. E. Lexical organization of nouns and verbs in the brain. Nature 349, 788-790 (1991).
38. Hickok, G. S. Computational neuroanatomy of speech production. Nat. Rev. Neurosci. 13, 135-145 (2012).
39. Pulvermüller, F. et al. Motor cortex maps articulatory features of speech sounds. Proc. Natl Acad. Sci. USA 103, 7865-7870 (2006).
40. Lotto, A. J., Hickok, G. S. & Holt, L. L. Reflections on mirror neurons and speech perception. Trends Cogn. Sci. 13, 110-114 (2009).
41. Indefrey, P. & Levelt, W. J. M. The spatial and temporal signatures of word production components. Cognition 92, 101-144 (2004).
42. Baron, S. G., Thompson-Schill, S. L., Weber, M. & Osherson, D. An early stage of conceptual combination: Superimposition of constituent concepts in left anterolateral temporal lobe. Cogn. Neurosci. 1, 44-51 (2010).
43. Olson, I. R., McCoy, D., Klobusicky, E. & Ross, L. A. Social cognition and the anterior temporal lobes: A review and theoretical framework. Soc. Cogn. Affect. Neurosci. 8, 123-133 (2013).
44. Butler, C. R., Brambati, S. M., Miller, B. L. & Gornoini, M. L. The neural correlates of verbal and nonverbal semantic processing deficits in neurodegenerative disease. Cogn. Behav. Neurol. 22, 73-80 (2009).
45. Jefferies, E. & Lambon Ralph, M. A. Semantic impairment in stroke aphasia versus semantic dementia: A case-series comparison. Brain 129, 2132-2147 (2006).
46. Jefferies, E. The neural basis of semantic cognition: Converging evidence from neuropsychology, neuroimaging and TMS. Cortex 49, 611-625 (2013).
47. Mirman, D. & Britt, A. E. What we talk about when we talk about access deficits. Philos. Trans. R. Soc. B Biol. Sci. 369, 1-14 (2014).
48. Badre, D. &Wagner, A. D. Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia 45, 2883-2901 (2007).
49. Thompson-Schill, S. L., Bedny, M. & Goldberg, R. F. The frontal lobes and the regulation of mental activity. Curr. Opin. Neurobiol. 15, 219-224 (2005).
50. Buxbaum, L. J. & Kalénine, S. Action knowledge, visuomotor activation, and embodiment in the two action systems. Ann. N. Y. Acad. Sci. 1191, 201-218 (2010).
51. Mirman, D. & Graziano, K. M. Damage to temporo-parietal cortex decreases incidental activation of thematic relations during spoken word comprehension. Neuropsychologia 50, 1990-1997 (2012).
52. Schwartz, M. F., Dell, G. S., Martin, N., Gahl, S. & Sobel, P. A case-series test of the interactive two-step model of lexical access: Evidence from picture naming. J. Mem. Lang. 54, 228-264 (2006).
53. Lambon Ralph, M. A., McClelland, J. L., Patterson, K. E., Galton, C. J. & Hodges, J. R. No right to speak? The relationship between object naming and semantic impairment: Neuropsychological evidence and a computational model. J. Cogn. Neurosci. 13, 341-356 (2001).
54. Schwartz, M. F. et al. A neuroanatomical dissociation for taxonomic and thematic knowledge in the human brain. Proc. Natl Acad. Sci. 108, 8520-8524 (2011).
55. Lambon Ralph, M. A. Neurocognitive insights on conceptual knowledge and its breakdown. Philos. Trans. R. Soc. B Biol. Sci. 369, 20120392 (2014).
56. Fedorenko, E., Duncan, J. & Kanwisher, N. Language-selective and domaingeneral regions lie side by side within Broca's area. Curr. Biol. 22, 2059-2062 (2012).
57. Keller, S. S., Crow, T., Foundas, A., Amunts, K. & Roberts, N. Broca's area: Nomenclature, anatomy, typology and asymmetry. Brain Lang. 109, 29-48 (2009).
58. Mirman, D. & Graziano, K. M. The neural basis of inhibitory effects of semantic and phonological neighbors in spoken word production. J. Cogn. Neurosci 25, 1504-1516 (2013).
59. Bozeat, S., Lambon Ralph, M. A., Patterson, K. E., Garrard, P. & Hodges, J. R. Non-verbal semantic impairment in semantic dementia. Neuropsychologia 38, 1207-1215 (2000).
60. Howard, D. & Patterson, K. E. Pyramids and Palm Trees: A Test of Semantic Access From Pictures and Words (Thames Valley Test Company, 1992).
61. Martin, N., Schwartz, M. F. & Kohen, F. P. Assessment of the ability to process semantic and phonological aspects of words in aphasia: A multi-measurement approach. Aphasiology 20, 154-166 (2006).
62. Freedman, M. L. & Martin, R. C. Dissociable components of short-term memory and their relation to long-term learning. Cogn. Neuropsychol. 18, 193-226 (2001).
63. Dunn, L. M. & Dunn, L. M. Examiner's Manual for the Peabody Picture Vocabulary Test-III (PPVT-III) (American Guidance Service, 1997).
64. Roach, A., Schwartz, M. F., Martin, N., Grewal, R. S. & Brecher, A. R. The Philadelphia naming test: Scoring and rationale. Clin. Aphasiol. 24, 121-133 (1996).
65. Martin, R. C., Shelton, J. R. & Yaffee, L. S. Language processing and working memory: Neuropsychological evidence for separate phonological and semantic capacities. J. Mem. Lang. 33, 83-111 (1994).
66. Kay, J., Lesser, R. & Coltheart, M. Psycholinguistic assessments of language processing in aphasia (PALPA): An introduction. Aphasiology 10, 159-180 (1996).
67. Zhang, Y., Kimberg, D. Y., Coslett, H. B., Schwartz, M. F. & Wang, Z. Multivariate lesion-symptom mapping using support vector regression. Hum. Brain Mapp. 35, 5861-5876 (2014).
68. Pillay, S. B., Stengel, B. C., Humphries, C., Book, D. S. & Binder, J. R. Cerebral localization of impaired phonological retrieval during rhyme judgment. Ann. Neurol. 76, 738-746 (2014).
69. Wakana, S. et al. Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36, 630-644 (2007).
70. Hua, K. et al. Tract probability maps in stereotaxic spaces: Analyses of white matter anatomy and tract-specific quantification. Neuroimage 39, 336-347 (2008).