An intracerebral exploration of functional connectivity during word production

  • Amandine Grappe
  • Sridevi V. Sarma
  • Pierre Sacré
  • Jorge González-Martínez
  • Catherine Liégeois-Chauvel
  • F.-Xavier AlarioEmail author


Language is mediated by pathways connecting distant brain regions that have diverse functional roles. For word production, the network includes a ventral pathway, connecting temporal and inferior frontal regions, and a dorsal pathway, connecting parietal and frontal regions. Despite the importance of word production for scientific and clinical purposes, the functional connectivity underlying this task has received relatively limited attention, and mostly from techniques limited in either spatial or temporal resolution. Here, we exploited data obtained from depth intra-cerebral electrodes stereotactically implanted in eight epileptic patients. The signal was recorded directly from various structures of the neocortex with high spatial and temporal resolution. The neurophysiological activity elicited by a picture naming task was analyzed in the time-frequency domain (10–150 Hz), and functional connectivity between brain areas among ten regions of interest was examined. Task related-activities detected within a network of the regions of interest were consistent with findings in the literature, showing task-evoked desynchronization in the beta band and synchronization in the gamma band. Surprisingly, long-range functional connectivity was not particularly stronger in the beta than in the high-gamma band. The latter revealed meaningful sub-networks involving, notably, the temporal pole and the inferior frontal gyrus (ventral pathway), and parietal regions and inferior frontal gyrus (dorsal pathway). These findings are consistent with the hypothesized network, but were not detected in every patient. Further research will have to explore their robustness with larger samples.


Speech Language Dorsal stream Ventral stream Stereo-electroencephalography Functional connectivity 



Research supported by grants ANR-11-LABX-0036 (BLRI), ANR-16-CONV-0002 (ILCB), by the Excellence Initiative of Aix-Marseille University (A∗MIDEX), and by a Kavli Neuroscience Discovery Institute postdoctoral fellowship awarded to P.S.

Compliance with Ethical Standards

Conflict of interests

The authors declare that they have no conflict of interest.


  1. Binder, J.R., & Desai, R.H. (2011). The neurobiology of semantic memory. Trends in Cognitive Sciences, 15 (11), 527–536. Scholar
  2. Bock, K. (1996). Language production: methods and methodologies. Psychonomic Bulletin & Review, 3(4), 395–421. Scholar
  3. Bourguignon, N.J. (2014). A rostro-caudal axis for language in the frontal lobe: the role of executive control in speech production. Neuroscience and Biobehavioral Reviews, 47, 431–444. Scholar
  4. Broca, P. (1861). Remarques sur le siège de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole) [Remarks on the seat of the faculty of articulated language, followed by an observation of aphemia (loss of speech)]. Bulletin et Mémoires de la Société Anatomique de Paris, 6, 330–357. Scholar
  5. Catani, M., & Mesulam, M. (2008). The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex, 44(8), 953–961. Scholar
  6. Catani, M., Jones, D.K., et al. (2005). Perisylvian language networks of the human brain. Annals of Neurology, 57(1), 8–16.CrossRefGoogle Scholar
  7. Clarke, A., & Tyler, L.K. (2015). Understanding what we see: how we derive meaning from vision. Trends in Cognitive Sciences, 19(11), 677–687. Scholar
  8. Collard, M.J., Fifer, M.S., Benz, H.L., McMullen, D.P., Wang, Y., Milsap, G.W., Korzeniewska, A., Crone, N.E. (2016). Cortical subnetwork dynamics during human language tasks. NeuroImage, 135, 261–272. Scholar
  9. Conant, D., Bouchard, K.E., Chang, E.F. (2014). Speech map in the human ventral sensory-motor cortex. Current Opinion in Neurobiology, 24, 63–67.CrossRefGoogle Scholar
  10. Conant, D.F., Bouchard, K.E., Leonard, M.K., Chang, E.F. (2018). Human sensorimotor cortex control of directly-measured vocal tract movements during vowel production. Journal of Neuroscience, 2382–17. Scholar
  11. Covington, N.V., & Duff, M.C. (2016). Expanding the language network: direct contributions from the hippocampus. Trends in Cognitive Sciences, 20(12), 869–870. Scholar
  12. Dell, G.S., Schwartz, M.F., Nozari, N., Faseyitan, O., Branch Coslett, H. (2013). Voxel-based lesion-parameter mapping: identifying the neural correlates of a computational model of word production. Cognition, 128(3), 380–396. Scholar
  13. Donner, T.H., & Siegel, M. (2011). A framework for local cortical oscillation patterns. Trends in Cognitive Sciences, 15(5), 191–199. Scholar
  14. Dubarry, A.S., Llorens, A., Trėbuchon, A, Carron, R., Liėgeois-Chauvel, C, Bėnar, C G, Alario, F.X. (2017). Estimating parallel processing in a language task using single-trial intracerebral electroencephalography. Psychological Science, 28(4), 414–426. Scholar
  15. Dumermuth, G., Gasser, T., Germann, P., Hecker, A., Herdan, M., Lange, B. (1977). Studies on EEG activities in the beta band. European Neurology, 16(1-6), 197–202. Scholar
  16. Engel, A.K., & Fries, P. (2010). Beta-band oscillations—signalling the status quo? Current Opinion in Neurobiology, 20(2), 156–165.CrossRefGoogle Scholar
  17. Ewald, A., Aristei, S., Nolte, G., Abdel-Rahman, R. (2012). Brain oscillations and functional connectivity during overt language production. Frontiers in Psychology, 3. .
  18. Flinker, A., Korzeniewska, A., Shestyuk, A.Y., Franaszczuk, P.J., Dronkers, N.F., Knight, R.T., Crone, N.E. (2015). Redefining the role of Broca’s area in speech. Proceedings of the National Academy of Sciences, 112(9), 2871–2875. Scholar
  19. Fridriksson, J., Yourganov, G., Bonilha, L., Basilakos, A., Den Ouden, D.B., Rorden, C. (2016). Revealing the dual streams of speech processing. Proceedings of the National Academy of Sciences, 113(52), 15,108–15,113. Scholar
  20. Friederici, A.D., & Singer, W. (2015). Grounding language processing on basic neurophysiological principles. Trends in Cognitive Sciences, 19(6), 1–10. Scholar
  21. Fries, P. (2015). Rhythms for cognition: communication through coherence. Neuron, 88(1), 220–235. Scholar
  22. Fuertinger, S., Horwitz, B., Simonyan, K. (2015). The functional connectome of speech control. PLOS Biology, 13(7), 1–31. Scholar
  23. Gaona, C.M., Sharma, M., Freudenburg, Z.V., Breshears, J.D., Bundy, D.T., Roland, J., Barbour, D.L., Schalk, G., Leuthardt, E.C. (2011). Nonuniform high-gamma (60-500 Hz) power changes dissociate cognitive task and anatomy in human cortex. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 31(6), 2091–2100. Scholar
  24. Geschwind, N. (1970). The organization of language and the brain. Science, 170(3961), 940–944. Scholar
  25. Goodale, M.A., & Milner, A.D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15(1), 20–25. Scholar
  26. Grill-Spector, K., & Weiner, K.S. (2014). The functional architecture of the ventral temporal cortex and its role in categorization. Nature Reviews Neuroscience, 15(8), 536–548. Scholar
  27. Hamamė, C M, Alario, F.X., Llorens, A., Liėgeois-Chauvel, C, Trébuchon-Da, F.A. (2014). High frequency gamma activity in the left hippocampus predicts visual object naming performance. Brain and Language, 135, 104–114. Scholar
  28. Han, Z., Ma, Y., Gong, G., Huang, R., Song, L., Bi, Y. (2016). White matter pathway supporting phonological encoding in speech production: a multi-modal imaging study of brain damage patients. Brain Structure and Function, 221(1), 577–589. Scholar
  29. Hassan, M., Benquet, P., Biraben, A., Berrou, C., Dufor, O., Wendling, F. (2015). Dynamic reorganization of functional brain networks during picture naming. Cortex, 73, 276–288. Scholar
  30. Herrmann, C.S., Grigutsch, M., Busch, N.A. (2005). EEG oscillations and wavelet analysis. In Handy, T.C. (Ed.) Event-related potentials: a methods handbook (pp. 229–259). Cambridge: MIT Press.Google Scholar
  31. Hickok, G. (2012). Computational neuroanatomy of speech production. Nature Reviews Neuroscience, 13, 135–45. Scholar
  32. Indefrey, P. (2011). The spatial and temporal signatures of word production components: a critical update. Frontiers in Psychology, 2, 255. Scholar
  33. Johnson, M.A., Thompson, S., Gonzalez-Martinez, J., Park, H.J., Bulacio, J., Najm, I., Kahn, K., Kerr, M., Sarma, S.V., Gale, J.T. (2014). Performing behavioral tasks in subjects with intracranial electrodes. Journal of Visualized Experiments: JoVE, 92, e51947. Scholar
  34. Korzeniewska, A., Franaszczuk, P.J., Crainiceanu, C.M., Kuł, R, Crone, NE. (2011). Dynamics of large-scale cortical interactions at high gamma frequencies during word production: event related causality (ERC) analysis of human electrocorticography (ECoG). NeuroImage, 56(4), 2218–2237. Scholar
  35. Lachaux, J.P., Axmacher, N., Mormann, F., Halgren, E., Crone, N.E. (2012). High-frequency neural activity and human cognition: past, present and possible future of intracranial EEG research. Progress in Neurobiology, 98(3), 279–301. Scholar
  36. Lambon-Ralph, M.A., Jefferies, E., Patterson, K., Rogers, T.T. (2016). The neural and computational bases of semantic cognition. Nature Reviews Neuroscience, 18, 42–55. Scholar
  37. Lichtheim, L. (1885). On aphasia. Brain, 7, 433–484. Scholar
  38. Liljestrȯm, M, Kujala, J., Stevenson, C., Salmelin, R. (2015). Dynamic reconfiguration of the language network preceding onset of speech in picture naming. Human Brain Mapping, 36(3), 1202–1216. Scholar
  39. Llorens, A., Trébuchon, A, Liégeois-Chauvel, C, Alario, F.X. (2011). Intra-cranial recordings of brain activity during language production. Frontiers in Psychology, 2. .
  40. Llorens, A., Trébuchon, A, Riès, S, Liégeois-Chauvel, C, Alario, F.X. (2014). How familiarization and repetition modulate the picture naming network. Brain and Language, 133, 47–58. Scholar
  41. Llorens, A., Dubarry, A.S., Trėbuchon, A, Chauvel, P., Alario, F.X., Liėgeois-Chauvel, C. (2016). Contextual modulation of hippocampal activity during picture naming. Brain and Language, 159, 92–101. Scholar
  42. Makris, N., & Pandya, D.N. (2009). The extreme capsule in humans and rethinking of the language circuitry. Brain Structure and Function, 213(3), 343. Scholar
  43. Margulies, D.S., & Petrides, M. (2013). Distinct parietal and temporal connectivity profiles of ventrolateral frontal areas involved in language production. Journal of Neuroscience, 33(42), 16,846–16,852. Scholar
  44. Maris, E. (2012). Statistical testing in electrophysiological studies. Psychophysiology, 49(4), 549–565. Scholar
  45. Maris, E., & Oostenveld, R. (2007). Nonparametric statistical testing of EEG and MEG data. Journal of Neuroscience Methods, 164(1), 177–190. Scholar
  46. Morlet, J. (1983). Sampling theory and wave propagation. In Chen, C (Ed.) Issues in acoustic signal – image processing and recognition, NATO ASI series (series f: computer and system sciences), (Vol. 1 pp. 233–261). Berlin: Springer.CrossRefGoogle Scholar
  47. Moscovitch, M., Cabeza, R., Winocur, G., Nadel, L. (2016). Episodic memory and beyond: the hippocampus and neocortex in transformation. Annual Review of Psychology, 67(1), 105–134. Scholar
  48. Papagno, C. (2011). Naming and the role of the uncinate fasciculus in language function. Current Neurology and Neuroscience Reports, 11(6), 553. Scholar
  49. Parlatini, V., Radua, J., Dell’Acqua, F., Leslie, A., Simmons, A., Murphy, D.G., Catani, M., de Schotten, M.T. (2017). Functional segregation and integration within fronto-parietal networks. NeuroImage, 146, 367–375. Scholar
  50. Petrides, M. (2014). Neuroanatomy of language regions of the human brain. London: Academic Press.Google Scholar
  51. Petrides, M., & Pandya, D.N. (2009). Distinct parietal and temporal pathways to the homologues of Broca’s area in the monkey. PLoS Biology, 7(8), e1000,170. Scholar
  52. Piai, V., Roelofs, A., Rommers, J., Maris, E. (2015). Beta oscillations reflect memory and motor aspects of spoken word production. Human Brain Mapping, 36(7), 2767–2780. Scholar
  53. Piai, V., Anderson, K.L., Lin, J.J., Dewar, C., Parvizi, J., Dronkers, N.F., Knight, R.T. (2016). Direct brain recordings reveal hippocampal rhythm underpinnings of language processing. Proceedings of the National Academy of Sciences, 113(40), 11,366–11,371. Scholar
  54. Poeppel, D., Emmorey, K., Hickok, G., Pylkkänen, L. (2012). Towards a new neurobiology of language. Journal of Neuroscience, 32(41), 14,125–14,131. Scholar
  55. Price, C.J. (2012). A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. NeuroImage, 62(2), 816–847. Scholar
  56. Riės, S K, Dhillon, R.K., Clarke, A., King-Stephens, D., Laxer, K.D., Weber, P.B., Kuperman, R.A., Auguste, K.I., Brunner, P., Schalk, G., Lin, J.J., Parvizi, J., Crone, N.E., Dronkers, N.F., Knight, R.T. (2017). Spatiotemporal dynamics of word retrieval in speech production revealed by cortical high-frequency band activity. Proceedings of the National Academy of Sciences, 114(23), E4530–E4538. Scholar
  57. Roelofs, A. (2014). A dorsal-pathway account of aphasic language production: the WEAVER++/ARC model. Cortex, 59, 33–48. Scholar
  58. Rogalsky, C., Poppa, T., Chen, K.H., Anderson, S.W., Damasio, H., Love, T., Hickok, G. (2015). Speech repetition as a window on the neurobiology of auditory-motor integration for speech: a voxel-based lesion symptom mapping study. Neuropsychologia, 71, 18–27. Scholar
  59. Rolston, JD, & Chang, EF. (in press). Critical language areas show increased functional connectivity in human cortex. Cerebral Cortex, 1–8.
  60. Saur, D., Kreher, B.W., Schnell, S., Kummerer, D., Kellmeyer, P., Vry, M.S., Umarova, R., Musso, M., Glauche, V., Abel, S., Huber, W., Rijntjes, M., Hennig, J., Weiller, C. (2008). Ventral and dorsal pathways for language. Proceedings of the National Academy of Sciences, 105(46), 18,035–18,040. Scholar
  61. Schwartz, M.F., Faseyitan, O., Kim, J., Coslett, H.B. (2012). The dorsal stream contribution to phonological retrieval in object naming. Brain: A Journal of Neurology, 135(12), 3799–3814. Scholar
  62. Sheldon, S., & Moscovitch, M. (2012). The nature and time-course of medial temporal lobe contributions to semantic retrieval: an fMRI study on verbal fluency. Hippocampus, 22(6), 1451– 1466.CrossRefGoogle Scholar
  63. Sheldon, S., McAndrews, M.P., Pruessner, J., Moscovitch, M. (2016). Dissociating patterns of anterior and posterior hippocampal activity and connectivity during distinct forms of category fluency. Neuropsychologia, 90, 148–158. Scholar
  64. Snodgrass, J.G., & Vanderwart, M. (1980). A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. Journal of Experimental Psychology: Human Learning and Memory, 6 (2), 174. Scholar
  65. Snodgrass, J.G., & Yuditsky, T. (1996). Naming times for the Snodgrass and Vanderwart pictures. Behavior Research Methods, 28(4), 516–536. Scholar
  66. Tremblay, P., & Dick, A.S. (2016). Broca and Wernicke are dead, or moving past the classic model of language neurobiology. Brain and Language, 162, 60–71. Scholar
  67. Uddin, L.Q., Supekar, K., Amin, H., Rykhlevskaia, E., Nguyen, D.A., Greicius, M.D., Menon, V. (2010). Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cerebral Cortex, 20(11), 2636–2646. Scholar
  68. Ueno, T., Saito, S., Rogers, T.T., Lambon Ralph, M.A. (2011). Lichtheim 2: synthesizing aphasia and the neural basis of language in a neurocomputational model of the dual dorsal-ventral language pathways. Neuron, 72(2), 385–396. Scholar
  69. Wang, X.J. (2010). Neurophysiological and computational principles of cortical rhythms in cognition. Physiological Reviews, 90(3), 1195–1268. Scholar
  70. Wang, H.E., Bénar, C G, Quilichini, P.P., Friston, K.J., Jirsa, V.K., Bernard, C. (2014). A systematic framework for functional connectivity measures. Frontiers in Neuroscience, 8, 405.PubMedPubMedCentralGoogle Scholar
  71. Wernicke, C. (1969). The symptom complex of aphasia. In Cohen, R, & Wartofsky, M (Eds.) Proceedings of the Boston colloquium for the philosophy of science 1966/1968., (Vol. 4 pp. 34–97). Dordrecht: Springer.
  72. Wu, Y., Sun, D., Wang, Y., Wang, Y., Wang, Y. (2016). Tracing short connections of the temporo-parieto-occipital region in the human brain using diffusion spectrum imaging and fiber dissection. Brain Research, 1646, 152–159. Scholar

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Authors and Affiliations

  1. 1.Institute for Computational MedicineJohns Hopkins UniversityBaltimoreUSA
  2. 2.Interfaculty Institute of BioengineeringEcole Polytechnique Fédérale de LausanneLausanneSwitzerland
  3. 3.Cleveland Clinic Neurological InstituteEpilepsy CenterClevelandUSA
  4. 4.INS, Institute of System NeuroscienceAix Marseille University, INSERMMarseilleFrance
  5. 5.LPCAix Marseille University, CNRSMarseilleFrance

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