Journal of Neurology

, 256:382

Is the left uncinate fasciculus essential for language?

A cerebral stimulation study
  • H. Duffau
  • P. Gatignol
  • S. Moritz-Gasser
  • E. Mandonnet


Despite a better understanding of the anatomy of the uncinate fasciculus (UF), its function remains poorly known. Our aim was to study the exact role of UF in language, and the possible existence of parallel distributed language networks within the “ventral stream”, underlaid by distinct subcortical tracts – namely the inferior occipito-temporal fasciculus (IOF) and UF.

We report a series of 13 patients operated on awake for a glioma involving the left anterior temporal lobe or the orbitofrontal area. We used intraoperative electrostimulation, to perform accurate and reliable anatomofunctional correlations both at cortical and subcortical levels. Using postoperative MRI, we correlated these functional findings with the anatomical locations of the sites where language disturbances were elicited by stimulation.

Intraoperative cortical stimulation found perilesional language sites in all cases. Subcortically, semantic paraphasia were induced in the 13 patients by stimulating the IOF, and phonological paraphasia were generated in 6 patients by stimulating the arcuate fasciculus. Interestingly, subcortical stimulation never elicited any language disturbances when performed at the level of the UF. Moreover, after a transient postoperative language deficit, all patients recovered, despite the removal of at least one part of the UF, as confirmed by control MRI.

We suggest that UF is not systematically essential for language. It can be explained by the fact that the “semantic ventral stream” might be constituted by at least two parallel pathways, i. e. a direct pathway underlaid by the IOF, crucial for language semantics, and an indirect pathway subserved by UF, which can be functionally compensated. However, we have to underline the fact not all language functions can be probed during surgery, and that more sensitive tasks have now to be added.

Key words

language uncinate fasciculus direct electrical stimulation connectivity brain mapping 


  1. 1.
    Bell BD, Hermann BP, Woodard AR, Jones JE, Rutecki PA, Sheth R, Dow CC, Seidenberg M (2001) Object naming and semantic knowledge in temporal lobe epilepsy. Neuropsychology 15:434–443PubMedCrossRefGoogle Scholar
  2. 2.
    Bello L, Gallucci M, Fava M, Carrabba G, Giussani C, Acerbi F, Baratta P, Songa V, Conte V, Branca V, Stocchetti N, Papagno C, Gaini SM (2007) Intraoperative subcortical language tract mapping guides surgical removal of gliomas involving speech areas. Neurosurgery 60:67–82PubMedCrossRefGoogle Scholar
  3. 3.
    Bookheimer S (2002) Functional MRI of language: new approaches to understanding the cortical organizaton of semantic processing. Annu Rev Neurosci 25:151–188PubMedCrossRefGoogle Scholar
  4. 4.
    Cappa SF, Frugoni M, Pasquali P (1998) Category-specific naming impairments for artefacts: a new case. Neurocase 4:391–397CrossRefGoogle Scholar
  5. 5.
    Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94PubMedCrossRefGoogle Scholar
  6. 6.
    Catani M, Jones DK, ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57:8–16PubMedCrossRefGoogle Scholar
  7. 7.
    Coppens JR, Mahaney KB, Abdulrauf SI (2005) An anteromedial approach to the temporal horn to avoid injury to the optic radiations fibers and uncinate fasciculus: anatomical and technical note. Neurosurg Focus 18:E3PubMedCrossRefGoogle Scholar
  8. 8.
    Crosby EC, Humphery T, Lauer EW (1962) Correlative anatomy of the Nervous system. New York: MacMillan, 357:402–409Google Scholar
  9. 9.
    Déjerine J (1895) Anatomie des centres nerveux. Vol 1. Paris: Rueff et Cie, pp 532–577Google Scholar
  10. 10.
    Desmurget M, Bonnetblanc F, Duffau H (2007) Contrasting acute and slowgrowing lesions: a new door to brain plasticity. Brain 130:898–914PubMedCrossRefGoogle Scholar
  11. 11.
    Devlin JT, Matthews PM, Rushworth MF (2003) Semantic processing in the left inferior prefrontal cortex: a combined functional magnetic resonance imaging and transcranial magnetic stimulation study. J Cogn Neurosci 15:71–84PubMedCrossRefGoogle Scholar
  12. 12.
    Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Bitar A, Sichez JP, Fohanno D (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomofunctional study. Brain 125:199–214PubMedCrossRefGoogle Scholar
  13. 13.
    Duffau H, Gatignol P, Denvil D, Lopes M, Capelle L (2003) The articulatory loop: study of the subcortical connectivity by electrostimulation. Neuroreport 14:2005–2008PubMedCrossRefGoogle Scholar
  14. 14.
    Duffau H, Gatignol P, Mandonnet E, Peruzzi P, Tzourio-Mazoyer N, Capelle L (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128:797–810PubMedCrossRefGoogle Scholar
  15. 15.
    Duffau H (2005) Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol 4:476–486PubMedCrossRefGoogle Scholar
  16. 16.
    Duffau H, Thiebaut de Schotten M, Mandonnet E (2008) White matter functional connectivity as an additional landmark for dominant temporal lobectomy. J Neurol Neurosurg Psychiatry 79:492–495PubMedCrossRefGoogle Scholar
  17. 17.
    Duffau H (2008) The anatomo-functional connectivity of language revisited. New insights provided by electrostimulation and tractography. Neuropsychologia 46:927–934PubMedCrossRefGoogle Scholar
  18. 18.
    Duffau H, Gatignol P, Mandonnet E, Capelle L, Taillandier L (2008) Contribution of intraoperative subcortical stimulation mapping of language pathways: a consecutive series of 115 patients operated on for a WHO grade II glioma in the left dominant hemisphere. J Neurosurg 109:461–471PubMedCrossRefGoogle Scholar
  19. 19.
    Ebeling U, von Cramon D (1992) Topography of the uncinate fascicle and adjacent temporal fiber tracts. Acta Neurochir (Wien) 115:143–148CrossRefGoogle Scholar
  20. 20.
    Gaffan D, Easton A, Parker A (2002) Interaction of inferior temporal cortex with frontal cortex and basal forebrain: double dissociation in strategy implementation and associative learning. J Neurosci 22:7288–7296PubMedGoogle Scholar
  21. 21.
    Gaillard R, Naccache L, Pinel P, Clémenceau S, Volle E, Hasboun D, Dupont S, Baulac M, Dehaene S, Adam C, Cohen L (2006) Direct intracranial, FMRI, and lesion evidence for the causal role of left inferotemporal cortex in reading. Neuron 50:191–204PubMedCrossRefGoogle Scholar
  22. 22.
    Gloor P (1997) The temporal lobe and the limbic system. New York: Oxford University PressGoogle Scholar
  23. 23.
    Glosser G, Salvucci AE, Chiaravalloti ND (2003) Naming and recognizing famous faces in temporal lobe epilepsy. Neurology 61:81–86PubMedGoogle Scholar
  24. 24.
    Goodglass H, Kaplan E (1972) The assessment of aphasia and related disorders. Philadelphia: Lea and FibigerGoogle Scholar
  25. 25.
    Halgren E, Wang C, Schomer DL, Knake S, Marinkovic K, Wu J, Ulbert I (2006) Processing stages underlying word recognition in the anteroventral temporal lobe. Neuroimage 30:1401–1413PubMedCrossRefGoogle Scholar
  26. 26.
    Hamberger MJ, Drake EB (2006) Cognitive functioning following epilepsy. Curr Neurol Neurosci Rep 6:319–326PubMedCrossRefGoogle Scholar
  27. 27.
    Jefferies E, Lambon Ralph MA (2006) Semantic impairment in stroke aphasia versus semantic dementia: a caseseries comparison. Brain 129: 2132–2147PubMedCrossRefGoogle Scholar
  28. 28.
    Kier EL, Staib LH, Davis LM, Bronen RA (2004) Anatomic dissection tractography: a new method for precise MR localization of white matter tracts. AJNR Am J Neuroradiol 25:670–676PubMedGoogle Scholar
  29. 29.
    Klinger J, Gloor P (1960) The connections of the amygdala and of the anterior temporal cortex in the human brain. J Comp Neurol 115:333–369CrossRefGoogle Scholar
  30. 30.
    Lambon Ralph MA, McClelland JL, Patterson K, Galton JC, Hodges JR (2001) No right to speak? The relationship between object naming and semantic impairment: neuropsychological evidence and a computational model. J Cogn Neurosci 13:341–356PubMedCrossRefGoogle Scholar
  31. 31.
    Lambon Ralph MA, Patterson K (2008) Generalization and differentiation in semantic memory: insights from semantic dementia. Ann N Y Acad Sci 1124:61–76PubMedCrossRefGoogle Scholar
  32. 32.
    Lu LH, Crosson B, Nadeau SE, Heilman KM, Gonzalez-Rothi LJ, Raymer A, Gilmore RL, Bauer RM, Roper SN (2002) Category-specific naming deficits for objects and actions: semantic atribute and grammatical role hypotheses. Neuropsychologia 40:1608–1621PubMedCrossRefGoogle Scholar
  33. 33.
    Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS Jr, Pandya DN (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex 15:854–869PubMedCrossRefGoogle Scholar
  34. 34.
    Mandonnet E, Nouet A, Gatignol P, Capelle L, Duffau H (2007) Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain 130:623–629PubMedCrossRefGoogle Scholar
  35. 35.
    Mazoyer B, Dehaene S, Tzourio N (1993) The cortical representation of speech. J Cogn neurosci 5:467–479CrossRefGoogle Scholar
  36. 36.
    Metz-Lutz M, Kremin H, Deloche G (1991) Standardisation d’un test de dénomination orale: contrôle des effets de l’âge, du sexe et du niveau de scolarité chez les sujets adultes normaux. Rev Neuropsychol 1:73–95Google Scholar
  37. 37.
    Nakamura M, McCarley RW, Kubicki M, Dickey CC, Niznikiewicz MA, Voglmaier MM, Seidman LJ, Maier SE, Westin CF, Kikinis R, Shenton ME (2005) Fronto-temporal disconnectivity in schizotypal personality disorder: a diffusion tensor imaging study. Biol Psychiatry 58:468–478PubMedCrossRefGoogle Scholar
  38. 38.
    Ojemann G, Ojemann J, Lettich E, Berger M (1989) Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71:316–326PubMedCrossRefGoogle Scholar
  39. 39.
    Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113PubMedCrossRefGoogle Scholar
  40. 40.
    Parker GJ, Luzzi S, Alexander DC, Wheeler-Kingshott CA, Ciccarelli O, Lambon Ralph MA (2005) Lateralization of ventral and dorsal auditorylanguage pathways in the human brain. Neuroimage 24:656–666PubMedCrossRefGoogle Scholar
  41. 41.
    Patterson K, Nestor PJ, Rogers TT (2007) Where do you know what you know? The representation of semantic knowledge in the human brain. Nat Rev Neurosci 8:976–987PubMedCrossRefGoogle Scholar
  42. 42.
    Pobric G, Jefferies E, Ralph MA (2007) Anterior temporal lobes mediate semantic representation: mimicking semantic dementia by using rTMS in normal participants. Proc Natl Acad Sci USA 104:20137–20141PubMedCrossRefGoogle Scholar
  43. 43.
    Price CJ, Devlin JT (2003) The myth of the visual word form area. Neuroimage 19:473–481PubMedCrossRefGoogle Scholar
  44. 44.
    Rodrigo S, Oppenheim C, Chassoux F, Golestani N, Cointepas Y, Poupon C, Semah F, Mangin JF, Le Bihan D, Meder JF (2007) Uncinate fasciculus fiber tracking in mesial temporal lobe epilepsy. Initial findings. Eur Radiol 17:1663–1668PubMedCrossRefGoogle Scholar
  45. 45.
    Scott SK, Blank CC, Rosen S, Wise RJ (2000) Identification of a pathway for intelligible speech in the left temporal lobe. Brain 123:2400–2406PubMedCrossRefGoogle Scholar
  46. 46.
    Szeszko PR, Robinson DG, Ashtari M, Vogel J, Betensky J, Sevy S, Ardekani BA, Lencz T, Malhotra AK, McCormack J, Miller R, Lim KO, Gunduz-Bruce H, Kane JM, Bilder RM (2008) Clinical and neuropsychological correlates of white matter abnormalities in recent onset schizophrenia. Neuropsychopharmacology 33:976–984PubMedCrossRefGoogle Scholar
  47. 47.
    Thompson-Schill SL, D’Esposito M, Aguirre GK, Farah MJ (1997) Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proc Natl Acad Sci USA 94:14792–14797PubMedCrossRefGoogle Scholar
  48. 48.
    Thompson-Schill SL, Aguirre GK, D’Esposito M, Farah MJ (1999) A neural basis for category and modality specificity of semantic knowledge. Neuropsychologia 37:671–676PubMedCrossRefGoogle Scholar
  49. 49.
    Tippett LJ, Glosser G, Farah MJ (1996) A category-specific naming impairment after temporal lobectomy. Neuropsychologia 34:134–146CrossRefGoogle Scholar
  50. 50.
    Vigneau M, Beaucousin V, Herve PY, Duffau H, Crivello F, Houdé O, Mazoyer B, Tzourio-Mazoyer N (2006) Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing. Neuroimage 30:1414–1432PubMedCrossRefGoogle Scholar
  51. 51.
    Wise RJ (2003) Language systems in normal and aphasic human subjects: functional imaging studies and inferences from animal studies. Br Med Bull 65:95–119PubMedCrossRefGoogle Scholar
  52. 52.
    Zahn R, Moll J, Krueger F, Huey ED, Garrido G, Grafman J (2007) Social concepts are represented in the superior anterior temporal cortex. Proc Natl Acad Sci USA 104:6430–6435PubMedCrossRefGoogle Scholar

Copyright information

© Steinkopff-Verlag 2009

Authors and Affiliations

  • H. Duffau
    • 1
    • 2
  • P. Gatignol
    • 2
  • S. Moritz-Gasser
    • 3
  • E. Mandonnet
    • 4
  1. 1.Dept. of Neurosurgery, Hôpital Gui de ChauliacCHU MontpellierMontpellierFrance
  2. 2.Laboratoire de Psychologie et de, Neurosciences CognitivesCNRS UMR 8189, Université René DescartesParis VFrance
  3. 3.Dept. of Neurology, Hôpital Gui de ChauliacCHU MontpellierMontpellierFrance
  4. 4.INSERM U678Hôpital de la SalpêtrièreParis, Cedex 13France

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