Brain Topography

, Volume 30, Issue 6, pp 747–756 | Cite as

Left Spatial Neglect Evoked by Electrostimulation of the Right Inferior Fronto-occipital Fasciculus

  • Guillaume Herbet
  • Yordanka N. Yordanova
  • Hugues Duffau
Original Paper


Left spatial neglect is a debilitating condition that may occur after lesion of many cortical territories in the right hemisphere. At the subcortical level, the second and third branches of the right superior longitudinal fasciculus has emerged as strong candidates in conveying information exchanges within the attention networks as their damage has been repeatedly associated to spatial neglect in neuromodulation and neuropsychological studies. Yet, a few cases of spatial neglect have also been observed after damage to the right inferior fronto-occipital fasciculus (IFOF), suggesting an involvement of this associative connectivity in spatial attention. Here we report three rare cases of patients having undergone a wide-awake craniotomy with direct electrostimulation for right temporal glioma. An intraoperative monitoring of spatial cognition was performed using a standard line bisection task. Responsive cortical sites were observed in the supramarginal gyrus and the posterior part of both the middle and superior temporal gyri. Critically, in all patients, significant rightward deviations were observed by the stimulation of the white matter deep in the temporal lobe, along the roof of the inferior horn of the lateral ventricle—a well-known anatomical landmark to identify the IFOF. Disconnection analyses confirmed the high probability of IFOF disconnection during neglect-related stimulations. Taken together, our findings provide support for a role of the right IFOF in spatial cognition. We discuss these results in the light of the newly discovered fronto-parietal connections of the IFOF and suggest that some subcomponents of this tract might be involved in between-system integration within the attention network.


Spatial neglect Spatial cognition Spatial attention White matter tracts Inferior fronto-occipital fasciculus 


Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Barbieri C, De Renzi E (1989) Patterns of neglect dissociation. Behav Neurol 2:13–24CrossRefPubMedGoogle Scholar
  2. Bartolomeo P (2013) Attention disorders after right brain damage: linving in halved worlds. Springer, LondonGoogle Scholar
  3. Bartolomeo P, Chokron S (2002) Orienting of attention in left unilateral neglect. Neurosci Biobehav Rev 26(2):217–234CrossRefPubMedGoogle Scholar
  4. Bartolomeo P, Thiebaut de Schotten M, Doricchi F (2007a) Left unilateral neglect as a disconnection syndrome. Cereb Cortex 17(11):2479–2490CrossRefPubMedGoogle Scholar
  5. Bartolomeo P, Thiebaut de Schotten M, Duffau H (2007b) Mapping of visuospatial functions during brain surgery: a new tool to prevent unilateral spatial neglect. Neurosurgery 61(6):E1340CrossRefPubMedGoogle Scholar
  6. Bartolomeo P, Thiebaut de Schotten M, Chica AB (2012) Brain networks of visuospatial attention and their disruption in visual neglect. Front Hum Neurosci 6:110PubMedPubMedCentralGoogle Scholar
  7. Binder J, Marshall R, Lazar R, Benjamin J, Mohr JP (1992) Distinct syndromes of hemineglect. Arch Neurol 49(11):1187–1194CrossRefPubMedGoogle Scholar
  8. Bressler SL, Menon V (2010) Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci 14(6):277–290CrossRefPubMedGoogle Scholar
  9. Brett M, Anton JL, Valabregue R, Poline JB (2002) Region of interest analysis using a SPM toolbox. Abstract presented at the 8th internation conference of functional mapping of the human brain, Sendai, JapanGoogle Scholar
  10. Carter AR, Astafiev SV, Lang CE, Connor LT, Rengachary J, Strube MJ, Pope DL, Shulman GL, Corbetta M (2010) Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke. Ann Neurol 67(3):365–375PubMedPubMedCentralGoogle Scholar
  11. Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17(1):77–94CrossRefPubMedGoogle Scholar
  12. Caverzasi E, Papinutto N, Amirbekian B, Berger MS, Henry RG (2014) Q-ball of inferior fronto-occipital fasciculus and beyond. PloS ONE 9(6):e100274CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chechlacz M, Rotshtein P, Bickerton WL, Hansen PC, Deb S, Humphreys GW (2010) Separating neural correlates of allocentric and egocentric neglect: distinct cortical sites and common white matter disconnections. Cogn Neuropsychol 27(3):277–303CrossRefPubMedGoogle Scholar
  14. Chechlacz M, Rotshtein P, Humphreys GW (2012) Neuroanatomical dissections of unilateral visual neglect symptoms: ALE meta-analysis of lesion-symptom mapping. Front Hum Neurosci 6:230CrossRefPubMedPubMedCentralGoogle Scholar
  15. Ciaraffa F, Castelli G, Parati EA, Bartolomeo P, Bizzi A (2013) Visual neglect as a disconnection syndrome? A confirmatory case report. Neurocase 19(4):351–359CrossRefPubMedGoogle Scholar
  16. Committeri G, Pitzalis S, Galati G, Patria F, Pelle G, Sabatini U, Castriota-Scanderbeg A, Piccardi L, Guariglia C, Pizzamiglio L (2007) Neural bases of personal and extrapersonal neglect in humans. Brain 130(Pt 2):431–441CrossRefPubMedGoogle Scholar
  17. Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215CrossRefPubMedGoogle Scholar
  18. Corbetta M, Shulman GL (2011) Spatial neglect and attention networks. Annu Rev Neurosci 34:569–599CrossRefPubMedPubMedCentralGoogle Scholar
  19. Crawford JR, Garthwaite PH (2007) Comparison of a single case to a control or normative sample in neuropsychology: development of a Bayesian approach. Cogn Neuropsychol 24(4):343–372CrossRefPubMedGoogle Scholar
  20. Desmurget M, Song Z, Mottolese C, Sirigu A (2013) Re-establishing the merits of electrical brain stimulation. Trends Cogn Sci 17(9):442–449CrossRefPubMedGoogle Scholar
  21. Doricchi F, Tomaiuolo F (2003) The anatomy of neglect without hemianopia: a key role for parietal-frontal disconnection? Neuroreport 14(17):2239–2243CrossRefPubMedGoogle Scholar
  22. Duffau H (2017) A two-level model of interindividual anatomo-functional variability of the brain and its implications for neurosurgery. Cortex 86:303–313CrossRefPubMedGoogle Scholar
  23. Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, Bitar A, Fohanno D (2002) Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125(Pt 1):199–214CrossRefPubMedGoogle Scholar
  24. 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(Pt 4):797–810CrossRefPubMedGoogle Scholar
  25. Hau J, Sarubbo S, Perchey G, Crivello F, Zago L, Mellet E, Jobard G, Joliot M, Mazoyer BM, Tzourio-Mazoyer N, Petit L (2016) Cortical terminations of the inferior fronto-occipital and uncinate fasciculi: anatomical stem-based virtual dissection. Front Neuroanat 10:58CrossRefPubMedPubMedCentralGoogle Scholar
  26. He BJ, Shulman GL, Snyder AZ, Corbetta M (2007a) The role of impaired neuronal communication in neurological disorders. Curr Opin Neurol 20(6):655–660CrossRefPubMedGoogle Scholar
  27. He BJ, Snyder AZ, Vincent JL, Epstein A, Shulman GL, Corbetta M (2007b) Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53(6):905–918CrossRefPubMedGoogle Scholar
  28. Heilman KM, Bowers D, Watson RT (1983) Performance on hemispatial pointing task by patients with neglect syndrome. Neurology 33(5):661–664CrossRefPubMedGoogle Scholar
  29. Herbet G, Maheu M, Costi E, Lafargue G, Duffau H (2016) Mapping neuroplastic potential in brain-damaged patients. Brain 139(Pt 3):829–844CrossRefPubMedGoogle Scholar
  30. Herbet G, Moritz-Gasser S, Duffau H (2017a) Direct evidence for the contributive role of the right inferior fronto-occipital fasciculus in non-verbal semantic cognition. Brain Struct Funct 222(4):1597–1610CrossRefPubMedGoogle Scholar
  31. Herbet G, Lafargue G, Duffau H (2017b) An atlas of neuroplastic potential in brain-damaged patients. Med Sci 33(1):84–86Google Scholar
  32. Husain M, Kennard C (1996) Visual neglect associated with frontal lobe infarction. J Neurol 243(9):652–657CrossRefPubMedGoogle Scholar
  33. Karnath HO, Ferber S, Himmelbach M (2001) Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 411(6840):950–953CrossRefPubMedGoogle Scholar
  34. Karnath HO, Fruhmann Berger M, Kuker W, Rorden C (2004) The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb Cortex 14(10):1164–1172CrossRefPubMedGoogle Scholar
  35. Karnath HO, Rorden C, Ticini LF (2009) Damage to white matter fiber tracts in acute spatial neglect. Cereb Cortex 19(10):2331–2337CrossRefPubMedPubMedCentralGoogle Scholar
  36. Karnath HO, Rennig J, Johannsen L, Rorden C (2011) The anatomy underlying acute versus chronic spatial neglect: a longitudinal study. Brain 134(Pt 3):903–912CrossRefPubMedGoogle Scholar
  37. Lunven M, Thiebaut de Schotten M, Bourlon C, Duret C, Migliaccio R, Rode G, Bartolomeo P (2015) White matter lesional predictors of chronic visual neglect: a longitudinal study. Brain 138(pt3):746–760CrossRefPubMedPubMedCentralGoogle Scholar
  38. Makris N, Kennedy DN, McInemey S, Sorengen AG, Wang R, Caviness VS Jr, Pandya DN (2005) Segmentation of subcomonents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex 15(6):854–869Google Scholar
  39. Mesulam MM (1998) From sensation to cognition. Brain 121(Pt 6):1013–1052CrossRefPubMedGoogle Scholar
  40. Mesulam MM (2015) Fifty years of disconnexion syndromes and the Geschwind legacy. Brain 138(Pt 9):2791–2799CrossRefPubMedGoogle Scholar
  41. Molenberghs P, Sale MV, Mattingley JB (2012) Is there a critical lesion site for unilateral spatial neglect? A meta-analysis using activation likelihood estimation. Front Hum Neurosci 6:78CrossRefPubMedPubMedCentralGoogle Scholar
  42. Moritz-Gasser S, Herbet G, Duffau H (2013) Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: a brain electrostimulation study. Neuropsychologia 51(10):1814–1822CrossRefPubMedGoogle Scholar
  43. Mort DJ, Malhotra P, Mannan SK, Rorden C, Pambakian A, Kennard C, Husain M (2003) The anatomy of visual neglect. Brain 126(Pt 9):1986–1997CrossRefPubMedGoogle Scholar
  44. Philippi CL, Mehta S, Grabowski T, Adolphs R, Rudrauf D (2009) Damage to association fiber tracts impairs recognition of the facial expression of emotion. J Neurosci 29(48):15089–15099CrossRefPubMedPubMedCentralGoogle Scholar
  45. Rech F, Herbet G, Moritz-Gasser S, Duffau H (2014) Disruption of bimanual movement by unilateral subcortical electrostimulation. Hum Brain Mapp 35(7):3439–3445CrossRefPubMedGoogle Scholar
  46. Rech F, Herbet G, Moritz-Gasser S, Duffau H (2016) Somatotopic organization of the white matter tracts underpinning motor control in humans: an electrical stimulation study. Brain Struct Funct 221 (7):3743–3753CrossRefPubMedGoogle Scholar
  47. Rengachary J, He BJ, Shulman GL, Corbetta M (2011) A behavioral analysis of spatial neglect and its recovery after stroke. Front Hum Neurosci 5:29CrossRefPubMedPubMedCentralGoogle Scholar
  48. Rojkova K, Volle E, Urbanski M, Humbert F, Dell’Acqua F, Thiebaut de Schotten M (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221(3):1751–1766CrossRefPubMedGoogle Scholar
  49. Roux FE, Dufor O, Lauwers-Cances V, Boukhatem L, Brauge D, Draper L, Lotterie JA, Demonet JF (2011) Electrostimulation mapping of spatial neglect. Neurosurgery 69(6):1218–1231CrossRefPubMedGoogle Scholar
  50. Samuelsson H, Jensen C, Ekholm S, Naver H, Blomstrand C (1997) Anatomical and neurological correlates of acute and chronic visuospatial neglect following right hemisphere stroke. Cortex 33(2):271–285CrossRefPubMedGoogle Scholar
  51. Sarubbo S, De Benedictis A, Maldonado IL, Basso G, Duffau H (2013) Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Struct Funct 218(1):21–37CrossRefPubMedGoogle Scholar
  52. Sarubbo S, De Benedictis A, Merler S, Mandonnet E, Balbi S, Granieri E, Duffau H (2015) Towards a functional atlas of human white matter. Hum Brain Mapp 36(8):3117–3136CrossRefPubMedGoogle Scholar
  53. Schmahmann JD, Pandya DN, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, Wedeen VJ (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130(Pt 3):630–653CrossRefPubMedGoogle Scholar
  54. Schucht P, Moritz-Gasser S, Herbet G, Raabe A, Duffau H (2013) Subcortical electrostimulation to identify network subserving motor control. Hum Brain Mapp 34(11):3023–3030. doi: 10.1002/hbm.22122 CrossRefPubMedGoogle Scholar
  55. Sharp DJ, Scott G, Leech R (2014) Network dysfunction after traumatic brain injury. Nat Rev Neurol 10(3):156–166CrossRefPubMedGoogle Scholar
  56. Suchan J, Umarova R, Schnell S, Himmelbach M, Weiller C, Karnath HO, Saur D (2014) Fiber pathways connecting cortical areas relevant for spatial orienting and exploration. Hum Brain Mapp 35(3):1031–1043CrossRefPubMedGoogle Scholar
  57. Tate MC, Herbet G, Moritz-Gasser S, Tate JE, Duffau H (2014) Probabilistic map of critical functional regions of the human cerebral cortex: Broca’s area revisited. Brain 137(Pt 10):2773–2782CrossRefPubMedGoogle Scholar
  58. Thiebaut de Schotten M, Urbanski M, Duffau H, Volle E, Levy R, Dubois B, Bartolomeo P (2005) Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309(5744):2226–2228CrossRefPubMedGoogle Scholar
  59. Thiebaut de Schotten M, Dell’Acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DG, Catani M (2011a) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246CrossRefPubMedGoogle Scholar
  60. Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’Acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DG, Catani M (2011b) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54(1):49–59CrossRefPubMedGoogle Scholar
  61. Thiebaut de Schotten M, Tomaiuolo F, Aiello M, Merola S, Silvetti M, Lecce F, Bartolomeo P, Doricchi F (2014) Damage to white matter pathways in subacute and chronic spatial neglect: a group study and 2 single-case studies with complete virtual “in vivo” tractography dissection. Cereb Cortex 24(3):691–706CrossRefPubMedGoogle Scholar
  62. Thiebaut de Schotten M, Dell’Acqua F, Ratiu P, Leslie A, Howells H, Cabanis E, Iba-Zizen MT, Plaisant O, Simmons A, Dronkers NF, Corkin S, Catani M (2015) From phineas gage and monsieur leborgne to H.M.: revisiting disconnection syndromes. Cereb Cortex 25(12):4812–4827CrossRefPubMedPubMedCentralGoogle Scholar
  63. Umarova RM, Saur D, Schnell S, Kaller CP, Vry MS, Glauche V, Rijntjes M, Hennig J, Kiselev V, Weiller C (2010) Structural connectivity for visuospatial attention: significance of ventral pathways. Cereb Cortex 20(1):121–129CrossRefPubMedGoogle Scholar
  64. Urbanski M, Thiebaut de Schotten M, Rodrigo S, Catani M, Oppenheim C, Touze E, Chokron S, Meder JF, Levy R, Dubois B, Bartolomeo P (2008) Brain networks of spatial awareness: evidence from diffusion tensor imaging tractography. J Neurol Neurosurg Psychiatry 79(5):598–601CrossRefPubMedGoogle Scholar
  65. Urbanski M, Thiebaut de Schotten M, Rodrigo S, Oppenheim C, Touze E, Meder JF, Moreau K, Loeper-Jeny C, Dubois B, Bartolomeo P (2011) DTI-MR tractography of white matter damage in stroke patients with neglect. Exp Brain Res 208(4):491–505CrossRefPubMedGoogle Scholar
  66. Vallar G (1998) Spatial hemineglect in Humans. Trends Cogn Sci 2(3):87–97CrossRefPubMedGoogle Scholar
  67. Vallar G, Perani D (1986) The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man. Neuropsychologia 24(5):609–622CrossRefPubMedGoogle Scholar
  68. Vallar G, Bello L, Bricolo E, Castellano A, Casarotti A, Falini A, Riva M, Fava E, Papagno C (2014) Cerebral correlates of visuospatial neglect: a direct cerebral stimulation study. Hum Brain Mapp 35(4):1334–1350CrossRefPubMedGoogle Scholar
  69. Verdon V, Schwartz S, Lovblad KO, Hauert CA, Vuilleumier P (2010) Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. Brain 133(Pt 3):880–894CrossRefPubMedGoogle Scholar
  70. Vossel S, Geng JJ, Fink GR (2014) Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neuroscientist 20(2):150–159CrossRefPubMedPubMedCentralGoogle Scholar
  71. Wang J, Tian Y, Wang M, Cao L, Wu H, Zhang Y, Wang K, Jiang T (2016) A lateralized top-down network for visuospatial attention and neglect. Brain Imaging Behav 10(4):1029–1037CrossRefPubMedGoogle Scholar
  72. Wu Y, Sun D, Wang Y, Wang Y (2016a) Subcomponents and connectivity of the inferior fronto-occipital fasciculus revealed by diffusion spectrum imaging fiber tracking. Front Neuroanat 10:88PubMedPubMedCentralGoogle Scholar
  73. Wu Y, Wang J, Zhang Y, Zheng D, Zhang J, Rong M, Wu H, Wang Y, Zhou K, Jiang T (2016b) The neuroanatomical basis for posterior superior parietal lobule control lateralization of visuospatial attention. Front Neuroanat 10:32PubMedPubMedCentralGoogle Scholar
  74. Yordanova NY, Duffau H, Herbet G (2017) Neural pathways for face-based mentalizing. Brain Struct Funct. doi: 10.1007/s00429-017-1388-0 PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Guillaume Herbet
    • 1
    • 2
    • 3
  • Yordanka N. Yordanova
    • 2
    • 4
  • Hugues Duffau
    • 1
    • 2
    • 3
  1. 1.Department of Neurosurgery, Gui de Chauliac HospitalMontpellier University Medical CenterMontpellierFrance
  2. 2.Institute for Neuroscience of Montpellier, INSERM 1051, Team “Plasticity of Central Nervous System, Human Stem Cells and Glial Tumors”, Saint Eloi HospitalMontpellier University Medical CenterMontpellierFrance
  3. 3.University of MontpellierMontpellierFrance
  4. 4.Department of Neurosurgery‘Percy’ Military HospitalClamartFrance

Personalised recommendations