Network dynamics of Broca’s area during word selection


Autoři: Christopher R. Conner aff001;  Cihan M. Kadipasaoglu aff001;  Harel Z. Shouval aff003;  Gregory Hickok aff004;  Nitin Tandon aff001
Působiště autorů: Vivian L Smith Department of Neurosurgery, University of Texas Medical School at Houston, Houston, TX, United States of America aff001;  Mischer Neuroscience Institute, Memorial Hermann Hospital, Houston, Texas, United States of America aff002;  Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, Houston, TX, United States of America aff003;  Department of Cognitive Sciences, University of California, Irvine, CA, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225756

Souhrn

Current models of word-production in Broca’s area (i.e. left ventro-lateral prefrontal cortex, VLPFC) posit that sequential and staggered semantic, lexical, phonological and articulatory processes precede articulation. Using millisecond-resolution intra-cranial recordings, we evaluated spatiotemporal dynamics and high frequency functional interconnectivity between left VLPFC regions during single-word production. Through the systematic variation of retrieval, selection, and phonological loads, we identified specific activation profiles and functional coupling patterns between these regions that fit within current psycholinguistic theories of word production. However, network interactions underpinning these processes activate in parallel (not sequentially), while the processes themselves are indexed by specific changes in network state. We found evidence that suggests that pars orbitalis is coupled with pars triangularis during lexical retrieval, while lexical selection is terminated via coupled activity with M1 at articulation onset. Taken together, this work reveals that speech production relies on very specific inter-regional couplings in rapid sequence in the language dominant hemisphere.

Klíčová slova:

Functional magnetic resonance imaging – Language – Left hemisphere – Phonemes – Phonology – Right hemisphere – Semantics – Speech


Zdroje

1. Broca P. Remarques sur le sie`ge de la faculte´ du langage articule´; suivies d’une observation d’aphemie. Bulletin de la Societe Anatomique. 1861;2:330–57.

2. Price CJ. The anatomy of language: contributions from functional neuroimaging. J Anat. 2000;197 Pt 3:335–59. Epub 2000/12/16. doi: 10.1046/j.1469-7580.2000.19730335.x 11117622; PubMed Central PMCID: PMC1468137.

3. Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME. Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature. 1988;331(6157):585–9. Epub 1988/02/18. doi: 10.1038/331585a0 3277066

4. Amunts K, Lenzen M, Friederici AD, Schleicher A, Morosan P, Palomero-Gallagher N, et al. Broca's region: novel organizational principles and multiple receptor mapping. PLoS Biol. 2010;8(9). Epub 2010/09/30. doi: 10.1371/journal.pbio.1000489 20877713; PubMed Central PMCID: PMC2943440.

5. Chang EF, Rieger JW, Johnson K, Berger MS, Barbaro NM, Knight RT. Categorical speech representation in human superior temporal gyrus. Nat Neurosci. 2011;13(11):1428–32. Epub 2010/10/05. doi: nn.2641 [pii] doi: 10.1038/nn.2641 20890293; PubMed Central PMCID: PMC2967728.

6. Sahin NT, Pinker S, Cash SS, Schomer D, Halgren E. Sequential processing of lexical, grammatical, and phonological information within Broca's area. Science. 2009;326(5951):445–9. Epub 2009/10/17. doi: 326/5951/445 [pii] doi: 10.1126/science.1174481 19833971

7. Heim S, Eickhoff SB, Ischebeck AK, Friederici AD, Stephan KE, Amunts K. Effective connectivity of the left BA 44, BA 45, and inferior temporal gyrus during lexical and phonological decisions identified with DCM. Hum Brain Mapp. 2009;30(2):392–402. Epub 2007/12/21. doi: 10.1002/hbm.20512 18095285

8. Badre D, Wagner AD. Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia. 2007;45(13):2883–901. Epub 2007/08/07. doi: 10.1016/j.neuropsychologia.2007.06.015 17675110

9. Gold BT, Balota DA, Jones SJ, Powell DK, Smith CD, Andersen AH. Dissociation of automatic and strategic lexical-semantics: functional magnetic resonance imaging evidence for differing roles of multiple frontotemporal regions. J Neurosci. 2006;26(24):6523–32. Epub 2006/06/16. doi: 10.1523/JNEUROSCI.0808-06.2006 16775140

10. Thompson-Schill SL, Bedny M, Goldberg RF. The frontal lobes and the regulation of mental activity. Curr Opin Neurobiol. 2005;15(2):219–24. Epub 2005/04/16. doi: 10.1016/j.conb.2005.03.006 15831406

11. Hagoort P. On Broca, brain, and binding: a new framework. Trends Cogn Sci. 2005;9(9):416–23. Epub 2005/08/02. doi: 10.1016/j.tics.2005.07.004 16054419

12. Bookheimer S. Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Annu Rev Neurosci. 2002;25:151–88. Epub 2002/06/08. doi: 10.1146/annurev.neuro.25.112701.142946 12052907

13. Pulvermuller F, Fadiga L. Active perception: sensorimotor circuits as a cortical basis for language. Nat Rev Neurosci. 2010;11(5):351–60. Epub 2010/04/13. doi: nrn2811 [pii] doi: 10.1038/nrn2811 20383203

14. Hickok G. Computational neuroanatomy of speech production. Nat Rev Neurosci. 2012;13(2):135–45. Epub 2012/01/06. doi: 10.1038/nrn3158 22218206

15. Flinker A, Korzeniewska A, Shestyuk AY, Franaszczuk PJ, Dronkers NF, Knight RT, et al. Redefining the role of Broca's area in speech. Proc Natl Acad Sci U S A. 2015;112(9):2871–5. doi: 10.1073/pnas.1414491112 25730850; PubMed Central PMCID: PMC4352780.

16. Poldrack RA, Wagner AD, Prull MW, Desmond JE, Glover GH, Gabrieli JD. Functional specialization for semantic and phonological processing in the left inferior prefrontal cortex. Neuroimage. 1999;10(1):15–35. Epub 1999/07/01. doi: 10.1006/nimg.1999.0441 10385578

17. Indefrey P, Levelt WJ. The spatial and temporal signatures of word production components. Cognition. 2004;92(1–2):101–44. Epub 2004/03/24. doi: 10.1016/j.cognition.2002.06.001 15037128

18. Indefrey P. The spatial and temporal signatures of word production components: a critical update. Frontiers in psychology. 2011;2:255. doi: 10.3389/fpsyg.2011.00255 22016740; PubMed Central PMCID: PMC3191502.

19. Chanceaux M, Vitu F, Bendahman L, Thorpe S, Grainger J. Word processing speed in peripheral vision measured with a saccadic choice task. Vision Res. 2012;56:10–9. doi: 10.1016/j.visres.2012.01.014 22306679

20. MacGregor LJ, Pulvermuller F, van Casteren M, Shtyrov Y. Ultra-rapid access to words in the brain. Nature communications. 2012;3:711. doi: 10.1038/ncomms1715 22426232; PubMed Central PMCID: PMC3543931.

21. Levelt WJ, Praamstra P, Meyer AS, Helenius P, Salmelin R. An MEG study of picture naming. J Cogn Neurosci. 1998;10(5):553–67. Epub 1998/11/06. doi: 10.1162/089892998562960 9802989

22. Levelt WJ, Roelofs A, Meyer AS. A theory of lexical access in speech production. Behav Brain Sci. 1999;22(1):1–38; discussion -75. Epub 2001/04/17. doi: 10.1017/s0140525x99001776 11301520

23. Salmelin R, Hari R, Lounasmaa OV, Sams M. Dynamics of brain activation during picture naming. Nature. 1994;368(6470):463–5. Epub 1994/03/31. doi: 10.1038/368463a0 8133893

24. Bouchard KE, Mesgarani N, Johnson K, Chang EF. Functional organization of human sensorimotor cortex for speech articulation. Nature. 2013;495(7441):327–32. Epub 2013/02/22. doi: 10.1038/nature11911 23426266; PubMed Central PMCID: PMC3606666.

25. Mesgarani N, Chang EF. Selective cortical representation of attended speaker in multi-talker speech perception. Nature. 2012;485(7397):233–6. Epub 2012/04/24. doi: 10.1038/nature11020 22522927

26. Edwards E, Nagarajan SS, Dalal SS, Canolty RT, Kirsch HE, Barbaro NM, et al. Spatiotemporal imaging of cortical activation during verb generation and picture naming. Neuroimage. 2010;50(1):291–301. Epub 2009/12/23. doi: 10.1016/j.neuroimage.2009.12.035 20026224; PubMed Central PMCID: PMC2957470.

27. Ries SK, Dhillon RK, Clarke A, King-Stephens D, Laxer KD, Weber PB, et al. Spatiotemporal dynamics of word retrieval in speech production revealed by cortical high-frequency band activity. Proc Natl Acad Sci U S A. 2017;114(23):E4530–E8. doi: 10.1073/pnas.1620669114 28533406; PubMed Central PMCID: PMC5468648.

28. Caramazza A. How many levels of processing are there in Lexical Access? Cognitive neuropsychology. 1997;14(1):177–208.

29. Dell GS. A spreading-activation theory of retrieval in sentence production. Psychological review. 1986;93(3):283–321. Epub 1986/07/01. 3749399

30. Dell GS, O'Seaghdha PG. Stages of lexical access in language production. Cognition. 1992;42(1–3):287–314. Epub 1992/03/01. doi: 10.1016/0010-0277(92)90046-k 1582160

31. Costafreda SG, Fu CH, Lee L, Everitt B, Brammer MJ, David AS. A systematic review and quantitative appraisal of fMRI studies of verbal fluency: role of the left inferior frontal gyrus. Hum Brain Mapp. 2006;27(10):799–810. doi: 10.1002/hbm.20221 16511886

32. Gough PM, Nobre AC, Devlin JT. Dissociating linguistic processes in the left inferior frontal cortex with transcranial magnetic stimulation. J Neurosci. 2005;25(35):8010–6. Epub 2005/09/02. doi: 10.1523/JNEUROSCI.2307-05.2005 16135758; PubMed Central PMCID: PMC1403818.

33. Voytek B, Kayser AS, Badre D, Fegen D, Chang EF, Crone NE, et al. Oscillatory dynamics coordinating human frontal networks in support of goal maintenance. Nat Neurosci. 2015. doi: 10.1038/nn.4071 26214371

34. Conner CR, Ellmore TM, Pieters TA, Disano MA, Tandon N. Variability of the Relationship between Electrophysiology and BOLD-fMRI across Cortical Regions in Humans. J Neurosci. 2011;31(36):12855–65. Epub 2011/09/09. doi: 31/36/12855 [pii] doi: 10.1523/JNEUROSCI.1457-11.2011 21900564

35. Wada J, Rasmussen TB. Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. J Neurosurg. 1960;17(2):166–282.

36. Snodgrass JG, Vanderwart M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. Journal of Experimental Psychology: Human Learning & Memory. 1980;6(2):174–215.

37. Brysbaert M, New B. Moving beyond Kucera and Francis: a critical evaluation of current word frequency norms and the introduction of a new and improved word frequency measure for American English. Behavior research methods. 2009;41(4):977–90. doi: 10.3758/BRM.41.4.977 19897807

38. Vaden KIH H.R.; Hickok G.S. Irvine Phonotactic Online Dictionary, Version 2.0. [Data file]. 2009.

39. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res. 1996;29(3):162–73. Epub 1996/06/01. doi: S0010480996900142 [pii]. doi: 10.1006/cbmr.1996.0014 8812068

40. Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999;9(2):179–94. Epub 1999/02/05. doi: S1053-8119(98)90395-0 [pii] doi: 10.1006/nimg.1998.0395 9931268

41. Tandon N. Cortical Mapping by Electrical Stimulation of Subdural Electrodes: Language areas. In: Luders H, editor. Textbook of Epilepsy Surgery: Informa Healthcare; 2008. p. 1001–15.

42. Pieters TA, Conner CR, Tandon N. Recursive grid partitioning on a cortical surface model: an optimized technique for the localization of implanted subdural electrodes. J Neurosurg. 2013. Epub 2013/03/19. doi: 10.3171/2013.2.JNS121450 23495883

43. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313(5793):1626–8. Epub 2006/09/16. doi: 313/5793/1626 [pii] doi: 10.1126/science.1128115 16973878; PubMed Central PMCID: PMC2628289.

44. Conner CR, Chen G, Pieters TA, Tandon N. Category Specific Spatial Dissociations of Parallel Processes Underlying Visual Naming. Cereb Cortex. 2013;[Epub ahead of print]. Epub 2013/05/23. doi: 10.1093/cercor/bht130 23696279

45. Bruns A, Eckhorn R, Jokeit H, Ebner A. Amplitude envelope correlation detects coupling among incoherent brain signals. Neuroreport. 2000;11(7):1509–14. Epub 2000/06/07. 10841367

46. Hipp JF, Hawellek DJ, Corbetta M, Siegel M, Engel AK. Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat Neurosci. 2012. Epub 2012/05/09. doi: 10.1038/nn.3101 22561454

47. Nir Y, Mukamel R, Dinstein I, Privman E, Harel M, Fisch L, et al. Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat Neurosci. 2008;11(9):1100–8. Epub 2009/01/23. doi: 10.1038/nn.2177 19160509; PubMed Central PMCID: PMC2642673.

48. Foster BL, Rangarajan V, Shirer WR, Parvizi J. Intrinsic and task-dependent coupling of neuronal population activity in human parietal cortex. Neuron. 2015;86(2):578–90. doi: 10.1016/j.neuron.2015.03.018 25863718; PubMed Central PMCID: PMC4409557.

49. Adhikari A, Sigurdsson T, Topiwala MA, Gordon JA. Cross-correlation of instantaneous amplitudes of field potential oscillations: a straightforward method to estimate the directionality and lag between brain areas. J Neurosci Methods. 2010;191(2):191–200. Epub 2010/07/06. doi: 10.1016/j.jneumeth.2010.06.019 20600317; PubMed Central PMCID: PMC2924932.

50. Kadipasaoglu CM, Conner CR, Baboyan VG, Rollo M, Pieters TA, Tandon N. Network dynamics of human face perception. PLoS One. 2017;12(11):e0188834. doi: 10.1371/journal.pone.0188834 29190811; PubMed Central PMCID: PMC5708727.

51. Sporns O. Networks of the Brain: MIT Press; 2010.

52. Whaley MLK C. M.; Cox S. J.; Tandon N.. Modulation of Orthographic Decoding by Frontal Cortex. Journal of Neuroscience. 2016;36(4). doi: 10.1523/JNEUROSCI.2985-15.2016 26818506

53. Rousseeuw PJ. A graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math. 1987;20:53–65.

54. d'Honincthun P, Pillon A. Verb comprehension and naming in frontotemporal degeneration: the role of the static depiction of actions. Cortex. 2008;44(7):834–47. Epub 2008/05/21. doi: S0010-9452(07)00128-1 [pii] doi: 10.1016/j.cortex.2007.04.003 18489963

55. Wilson SM, Isenberg AL, Hickok G. Neural correlates of word production stages delineated by parametric modulation of psycholinguistic variables. Hum Brain Mapp. 2009;30(11):3596–608. Epub 2009/04/15. doi: 10.1002/hbm.20782 19365800; PubMed Central PMCID: PMC2767422.

56. van den Heuvel MP, Sporns O. Rich-club organization of the human connectome. J Neurosci. 2011;31(44):15775–86. Epub 2011/11/04. doi: 10.1523/JNEUROSCI.3539-11.2011 22049421

57. Snyder HR, Hutchison N, Nyhus E, Curran T, Banich MT, O'Reilly RC, et al. Neural inhibition enables selection during language processing. Proc Natl Acad Sci U S A. 2010;107(38):16483–8. Epub 2010/09/04. doi: 1002291107 [pii] doi: 10.1073/pnas.1002291107 20813959

58. Koechlin E, Summerfield C. An information theoretical approach to prefrontal executive function. Trends Cogn Sci. 2007;11(6):229–35. doi: 10.1016/j.tics.2007.04.005 17475536

59. Sakai K, Passingham RE. Prefrontal interactions reflect future task operations. Nat Neurosci. 2003;6(1):75–81. Epub 2002/12/07. doi: 10.1038/nn987 12469132

60. Kadipasaoglu CM, Conner CR, Whaley ML, Baboyan VG, Tandon N. Category-Selectivity in Human Visual Cortex Follows Cortical Topology: A Grouped icEEG Study. PLoS One. 2016;11(6):e0157109. doi: 10.1371/journal.pone.0157109 27272936; PubMed Central PMCID: PMC4896492.

61. Bar M, Kassam KS, Ghuman AS, Boshyan J, Schmid AM, Dale AM, et al. Top-down facilitation of visual recognition. Proc Natl Acad Sci U S A. 2006;103(2):449–54. doi: 10.1073/pnas.0507062103 16407167; PubMed Central PMCID: PMC1326160.

62. Dell GS, Chang F, Griffin ZM. Connectionist Models of Language Production: Lexical Access and Grammatical Encoding Cogntive Science. 1999;24(4):517–42.

63. Price CJ, Devlin JT, Moore CJ, Morton C, Laird AR. Meta-analyses of object naming: effect of baseline. Hum Brain Mapp. 2005;25(1):70–82. Epub 2005/04/23. doi: 10.1002/hbm.20132 15846820

64. Margulies DS, Petrides M. Distinct parietal and temporal connectivity profiles of ventrolateral frontal areas involved in language production. J Neurosci. 2013;33(42):16846–52. doi: 10.1523/JNEUROSCI.2259-13.2013 24133284

65. Dronkers NF. A new brain region for coordinating speech articulation. Nature. 1996;384(6605):159–61. Epub 1996/11/14. doi: 10.1038/384159a0 8906789

66. Friederici AD. What's in control of language? Nat Neurosci. 2006;9(8):991–2. Epub 2006/07/28. doi: 10.1038/nn0806-991 16871165

67. Hickok G, Houde J, Rong F. Sensorimotor integration in speech processing: computational basis and neural organization. Neuron. 2011;69(3):407–22. Epub 2011/02/15. doi: S0896-6273(11)00067-5 [pii] doi: 10.1016/j.neuron.2011.01.019 21315253; PubMed Central PMCID: PMC3057382.

68. Averbeck BB, Latham PE, Pouget A. Neural correlations, population coding and computation. Nat Rev Neurosci. 2006;7(5):358–66. doi: 10.1038/nrn1888 16760916

69. Belitski A, Gretton A, Magri C, Murayama Y, Montemurro MA, Logothetis NK, et al. Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information. J Neurosci. 2008;28(22):5696–709. doi: 10.1523/JNEUROSCI.0009-08.2008 18509031

70. Gawne TJ, Kjaer TW, Hertz JA, Richmond BJ. Adjacent visual cortical complex cells share about 20% of their stimulus-related information. Cereb Cortex. 1996;6(3):482–9. doi: 10.1093/cercor/6.3.482 8670673

71. Gawne TJ, Richmond BJ. How independent are the messages carried by adjacent inferior temporal cortical neurons? J Neurosci. 1993;13(7):2758–71. doi: 10.1523/JNEUROSCI.13-07-02758.1993 8331371

72. Kohn A, Smith MA. Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J Neurosci. 2005;25(14):3661–73. doi: 10.1523/JNEUROSCI.5106-04.2005 15814797

73. Poort J, Roelfsema PR. Noise correlations have little influence on the coding of selective attention in area V1. Cereb Cortex. 2009;19(3):543–53. doi: 10.1093/cercor/bhn103 18552357; PubMed Central PMCID: PMC2638816.

74. Reich DS, Mechler F, Victor JD. Independent and redundant information in nearby cortical neurons. Science. 2001;294(5551):2566–8. doi: 10.1126/science.1065839 11752580

75. Zohary E, Shadlen MN, Newsome WT. Correlated neuronal discharge rate and its implications for psychophysical performance. Nature. 1994;370(6485):140–3. doi: 10.1038/370140a0 8022482

76. Friston K. Hierarchical models in the brain. PLoS Comput Biol. 2008;4(11):e1000211. Epub 2008/11/08. doi: 10.1371/journal.pcbi.1000211 18989391; PubMed Central PMCID: PMC2570625.

77. Badre D, D'Esposito M. Is the rostro-caudal axis of the frontal lobe hierarchical? Nat Rev Neurosci. 2009;10(9):659–69. doi: 10.1038/nrn2667 19672274; PubMed Central PMCID: PMC3258028.


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