Stimulation mapping of white matter tracts to study brain functional connectivity

Nature Reviews Neurology

Volumn 11, Issue 5, 2015, Pages 255-265

  Duffau, Hugues ^a  

^a GUI DE CHAULIAC HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATTENTION; BRAIN FUNCTION; BRAIN FUNCTIONAL CONNECTIVITY; BRAIN MAPPING; BRAIN SURGERY; COGNITIVE REHABILITATION; CONSCIOUSNESS; DEPTH PERCEPTION; EXECUTIVE FUNCTION; HUMAN; IN VIVO STUDY; LANGUAGE ABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE TRACT; NEUROLOGY; PRIORITY JOURNAL; PSYCHIATRY; REVIEW; SENSORIMOTOR FUNCTION; SOCIAL COGNITION; WHITE MATTER; WORKING MEMORY; BRAIN NEOPLASMS; CONNECTOME; ELECTROSTIMULATION; GLIOMA; MENTAL FUNCTION; NEUROSURGERY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; SENSORIMOTOR CORTEX; VISUAL SYSTEM;

BRAIN NEOPLASMS; CONNECTOME; ELECTRIC STIMULATION; GLIOMA; HUMANS; MAGNETIC RESONANCE IMAGING; MENTAL PROCESSES; NEURAL PATHWAYS; NEUROSURGICAL PROCEDURES; SENSORIMOTOR CORTEX; VISUAL PATHWAYS; WHITE MATTER;

EID: 84929270456     PISSN: 17594758     EISSN: 17594766     Source Type: Journal    
DOI: 10.1038/nrneurol.2015.51     Document Type: Review

References (114)

1. Lashley, K. In search of the engram. In Society of Experimental Biology Symposium, No. 4: Psychological Mechanisms in Animal Behaviour 454-480 (Cambridge University Press, 1950).
2. McClelland, J. J. & Rogers, T. T. The parallel distributed processing approach to semantic cognition. Nat. Rev. Neurosci. 4, 310-322 (2003).
3. Plaut, D. C., McClelland, J. L., Seidenberg, M. S. & Patterson K. Understanding normal and impaired word reading: computational principles in quasi-regular domains. Psychol. Rev. 103, 56-115 (1996).
4. Shallice, T. From Neuropsychology to Mental Structure (Cambridge University Press, 1988).
5. Ueno, T., Saito, S., Rogers, T. T. & Lambon Ralph, M. A. Lichtheim 2: synthesizing aphasia and the neural basis of language in a neurocomputational model of the dual dorsal-ventral language pathways. Neuron 72, 385-396 (2011).
6. Sporns, O. The human connectome: origins and challenges. Neuroimage 80, 53-61 (2013).
7. Honey, C. J., Kötter, R., Breakspear, M. & Sporns, O. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc. Natl Acad. Sci. USA 104, 10240-10245 (2007).
8. Basset, D. S. & Bullmore, E. T. Human brain networks in health and disease. Curr. Opin. Neurol. 22, 340-347 (2009).
9. Hutchison, R. M. et al. Dynamic functional connectivity: promise, issues, and interpretations. Neuroimage 80, 360-378 (2013).
10. Duffau, H. The huge plastic potential of adult brain and the role of connectomics: new insights provided by serial mappings in glioma surgery. Cortex 58, 325-337 (2014).
11. Fernandez-Miranda, J. C. et al. High-definition fiber tractography of the human brain: neuroanatomical validation and neurosurgical applications. Neurosurgery 71, 430-453 (2012).
12. Vergani, F. et al. White matter connections of the supplementary motor area in humans. J. Neurol. Neurosurg. Psychiatry 85, 1377-1385 (2014).
13. Van Essen, D. C. et al. The Human Connectome Project: a data acquisition perspective. Neuroimage 62, 2222-2231 (2012).
14. Smith, S. M. et al. Functional connectomics from resting-state fMRI. Trends Cogn. Sci. 17, 666-682 (2013).
15. Rorden, C., Fridriksson, J. & Karnath, H. O. An evaluation of traditional and novel tools for lesion behavior mapping. Neuroimage 44, 1355-1362 (2009).
16. Thompson, R. H. & Swanson, L. W. Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc. Natl Acad. Sci. USA 107, 15235-15239 (2010).
17. Micheva, K. D., Busse, B., Weiler, N. C., O'Rourke, N. & Smith, S. J. Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. Neuron 68, 639-653 (2010).
18. Leergaard, T. B., Hilgetag, C. C. & Sporns, O. Mapping the connectome: multi-level analysis of brain connectivity. Front. Neuroinform. 6, 14 (2012).
19. Catani, M., Thiebaut de Schotten, M., Slater, D. & Dell'Acqua, F. Connectomic approaches before the connectome. Neuroimage 80, 2-13 (2013).
20. Duffau, H. The "frontal syndrome" revisited: lessons from electrostimulation mapping studies. Cortex 48, 120-131 (2012).
21. Duffau, H. & Taillandier, L. New concepts in the management of diffuse low-grade gliomas: proposal of a multistage and individualized therapeutic approach. Neuro Oncol. 17, 332-342 (2014).
22. Duffau, H. (Ed.). Brain Mapping: From Neural Basis of Cognition to Surgical Applications (Springer, 2011).
23. Duffau, H., Gatignol, P., Mandonnet, E., Capelle, L. & Taillandier, L. Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with grade II glioma in the left dominant hemisphere. J. Neurosurg. 109, 461-471 (2008).
24. Mandonnet, E., Winkler, P. A. & Duffau, H. Direct electrical stimulation as an input gate into brain functional networks: principles, advantages and limitations. Acta Neurochir. (Wien) 152, 185-193 (2010).
25. Logothetis, N. K. et al. The effects of electrical microstimulation on cortical signal propagation. Nat. Neurosci. 13, 1283-1291 (2010).
26. Bello, L. et al. Motor and language DTI fiber tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 39, 369-382 (2008).
27. Duffau, H. et al. New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical stimulations. Brain 128, 797-810 (2005).
28. Ius, T., Angelini, E., Thiebaut de Schotten, M., Mandonnet, E. & Duffau, H. Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a "minimal common brain". Neuroimage 56, 992-1000 (2011).
29. Duffau, H. et al. Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J. Neurosurg. 98, 764-778 (2003).
30. Maldonado, I. L. et al. Surgery for gliomas involving the left inferior parietal lobule: new insights into the functional anatomy provided by stimulation mapping in awake patients. J. Neurosurg. 115, 770-779 (2011).
31. Schucht, P., Moritz-Gasser, S., Herbet, G., Raabe, A. & Duffau, H. Subcortical electrostimulation to identify network subserving motor control. Hum. Brain Mapp. 34, 3023-3030 (2013).
32. Rech, F., Herbet, G., Moritz-Gasser, S. & Duffau, H. Disruption of bimanual movement by unilateral subcortical stimulation. Hum. Brain Mapp. 35, 3439-3445 (2014).
33. Kinoshita, M., Menjot de Champfleur, N., Deverdun, J., Herbet, G. & Duffau, H. Role of fronto-striatal tract and frontal aslant tract in movement and speech: an axonal mapping study. Brain Struct. Funct. http://dx.doi.org/10.1007/s00429-014-0863-0.
34. Alexander, G. E. & Crutcher, M. D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13, 266-271 (1990).
35. Almairac, F., Herbet, G., Moritz-Gasser, S. & Duffau, H. Parietal network underlying movement control: disturbances during subcortical electrostimulation. Neurosurg. Rev. 37, 513-516 (2014).
36. Filimon, F. Human cortical control of hand movements: parietofrontal networks for reaching, grasping, and pointing. Neuroscientist 16, 388-407 (2010).
37. Fogassi, L. & Luppino, G. Motor functions of the parietal lobe. Curr. Opin. Neurobiol. 15, 626-631 (2005).
38. Jackson, S. R. et al. There may be more to reaching than meets the eye: re-thinking optic ataxia. Neuropsychologia 47, 1397-1408 (2009).
39. Duffau, H., Velut, S., Mitchell, M. C., Gatignol, P. & Capelle, L. Intra-operative mapping of the subcortical visual pathways using direct electrical stimulations. Acta Neurochir. (Wien) 146, 265-269 (2004).
40. Steňo, A. et al. Direct electrical stimulation of the optic radiation in patients with covered eyes. Neurosurg. Rev. 37, 527-533 (2014).
41. Gras-Combes, G., Moritz-Gasser, S., Herbet, G. & Duffau, H. Intraoperative subcortical electrical mapping of optic radiations in awake surgery for glioma involving visual pathways. J. Neurosurg. 117, 466-473 (2012).
42. Fernández Coello, A., Duvaux, S., De Benedictis, A., Matsuda, R. & Duffau, H. Involvement of the right inferior longitudinal fascicle in visual hemiagnosia: a brain stimulation mapping study. J. Neurosurg. 118, 202-205 (2013).
43. Thiebaut de Schotten, M. et al. Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science 309, 2226-2228 (2005).
44. Spena, G., Gatignol, P., Capelle, L. & Duffau, H. Superior longitudinal fasciculus subserves vestibular network in humans. Neuroreport 17, 1403-1406 (2006).
45. Duffau, H., Moritz-Gasser, S. & Mandonnet, E. A re-examination of neural basis of language processing: proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming. Brain Lang. 131, 1-10 (2014).
46. Hickok, G. & Poeppel, D. The cortical organization of speech processing. Nat. Rev. Neurosci. 8, 393-402 (2007).
47. Scott, S. K., Blank, C. C., Rosen, S. & Wise, R. J. Identification of a pathway for intelligible speech in the left temporal lobe. Brain 12, 2400-2406 (2000).
48. Weiller, C., Bormann, T., Saur, D., Musso, M. & Rijntjes, M. How the ventral pathway got lost: and what its recovery might mean. Brain. Lang. 118, 29-39 (2011).
49. Mandonnet, E., Gatignol, P. & Duffau, H. Evidence for an occipito-temporal tract underlying visual recognition in picture naming. Clin. Neurol. Neurosurg. 111, 601-605 (2009).
50. Gil Robles, S. et al. Double dissociation between visual recognition and picture naming: a study of the visual language connectivity using tractography and brain stimulation. Neurosurgery 72, 678-686 (2013).
51. Chan-Seng, E., Moritz-Gasser, S. & Duffau, H. Awake mapping for low-grade gliomas involving the left sagittal stratum: anatomofunctional and surgical considerations. J. Neurosurg. 120, 1069-1077 (2014).
52. Saur, D. et al. Ventral and dorsal pathways for language. Proc. Natl Acad. Sci. USA 105, 18035-18040 (2008).
53. Maldonado, I. L., Moritz-Gasser, S. & Duffau, H. Does the left superior longitudinal fascicle subserve language semantics? A brain electrostimulation study. Brain Struct. Funct. 216, 263-264 (2011).
54. Catani, M., Jones, D. K. & ffytche, D. H. Perisylvian language networks of the human brain. Ann. Neurol. 57, 8-16 (2005).
55. Duffau, H. et al. Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. Brain 125, 199-214 (2002).
56. Martino, J. et al. Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Struct. Funct. 218, 105-121 (2013).
57. Moritz-Gasser, S. & Duffau, H. The anatomo-functional connectivity of word repetition: insights provided by awake brain tumor surgery. Front. Hum. Neurosci. 7, 405 (2013).
58. Vigneau, M. et al. Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30, 1414-1432 (2006).
59. van Geemen, K., Herbet, G., Moritz-Gasser, S. & Duffau, H. Limited plastic potential of the left ventral premotor cortex in speech articulation: evidence from intraoperative awake mapping in glioma patients. Hum. Brain Mapp. 35, 1587-1596 (2014).
60. Duffau, H., Gatignol, P., Denvil, D., Lopes, M. & Capelle, L. The articulatory loop: study of the subcortical connectivity by electrostimulation. Neuroreport 14, 2005-2008 (2003).
61. Tate, M. C., Herbet, G., Moritz-Gasser, S., Tate, J. E. & Duffau, H. Probabilistic map of critical functional regions of the human cerebral cortex: Broca's area revisited. Brain 137, 2773-2782 (2014).
62. Duffau, H., Herbet, G. & Moritz-Gasser, S. Toward a pluri-component, multimodal, and dynamic organization of the ventral semantic stream in humans: lessons from stimulation mapping in awake patients. Front. Syst. Neurosci. 7, 44 (2013).
63. Martino, J., Brogna, C., Gil Robles, S., Vergani, F. & Duffau, H. Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46, 691-699 (2010).
64. Sarubbo, S., De Benedictis, A., Maldonado, I. L., Basso, G. & Duffau, H. Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle. Brain Struct. Funct. 218, 21-37 (2013).
65. 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).
66. Holland, R. & Lambon-Ralph, M. A. The anterior temporal lobe semantic hub is a part of the language neural network: selective disruption of irregular past tense verb by rTMS. Cereb. Cortex 20, 2771-2775 (2010).
67. Lambon Ralph, M. A., Sage, K., Jones, R. W. & Mayberry, E. J. Coherent concepts are computed in the anterior temporal lobes. Proc. Natl Acad. Sci. USA 107, 2717-2722 (2010).
68. Lambon Ralph, M. Neurocognitive insights on conceptual knowledge and its breakdown. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20120392 (2013).
69. Mandonnet, E., Nouet, A., Gatignol, P., Capelle, L. & Duffau, H. Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain 130, 623-629 (2007).
70. Duffau, H., Gatignol, P., Moritz-Gasser, S. & Mandonnet, E. Is the left uncinate fasciculus essential for language? A cerebral stimulation study. J. Neurol. 256, 382-389 (2009).
71. Han, Z. et al. White matter structural connectivity underlying semantic processing: evidence from brain damaged patients. Brain 136, 2952-2965 (2013).
72. Papagno, C. et al. What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain 134, 405-414 (2011).
73. Binney, R. J., Parker, G. J. & Lambon Ralph, M. A. Convergent connectivity and graded specialization in the rostral human temporal lobe as revealed by diffusion-weighted imaging probabilistic tractography. J. Cogn. Neurosci. 24, 1998-2014 (2012).
74. Jefferies, E. & Lambon Ralph, M. A. Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. Brain 129, 2132-2147 (2006).
75. Makris, N. et al. Human middle longitudinal fascicle: segregation and behavioral-clinical implications of two distinct fiber connections linking temporal pole and superior temporal gyrus with the angular gyrus or superior parietal lobule using multi-tensor tractography. Brain Imaging Behav. 7, 335-352 (2013).
76. De Witt Hamer, P., Moritz-Gasser, S., Gatignol, P. & Duffau, H. Is the human left middle longitudinal fascicle essential for language? A brain electrostimulation study. Hum. Brain Mapp. 32, 962-973 (2011).
77. Vidorreta, J. G., Garcia, R., Moritz-Gasser, S. & Duffau, H. Double dissociation between syntactic gender and picture naming processing: a brain stimulation mapping study. Hum. Brain Mapp. 32, 331-340 (2011).
78. Shimotake, A. et al. Direct exploration of the role of the ventral anterior temporal lobe in semantic memory: cortical stimulation and local field potential evidence from subdural grid electrodes. Cereb. Cortex http://dx.doi.org/10.1093/cercor/bhu262.
79. Abel, T. J. et al. Direct physiologic evidence of a heteromodal convergence region for proper naming in human left anterior temporal lobe. J. Neurosci. 35, 1513-1520 (2015).
80. Herbet, G., Lafargue, G., Moritz-Gasser, S., Bonnetblanc, F. & Duffau, H. Interfering with the neural activity of mirror-related frontal areas impairs mentalistic inferences. Brain Struct. Funct. http://dx.doi.org/10.1007/s00429-014-0777-x.
81. Herbet, G. et al. Inferring a dual-stream model of mentalizing from associative white matter fiber disconnection. Brain 137, 944-959 (2014).
82. Catani, M. & ffytche, D. H. The rises and falls of disconnection syndromes. Brain 128, 2224-2239 (2005).
83. Makris, N. et al. Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb. Cortex 15, 854-869 (2005).
84. Greicius, M. D., Supekar, K., Menon, V. & Dougherty, R. F. Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb. Cortex 19, 72-78 (2009).
85. van den Heuvel, M., Mandl, R., Luigjes, J. & Hulshoff Pol, H. Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J. Neurosci. 28, 10844-10851 (2008).
86. ffytche, D. H. & Catani, M. Beyond localization: from hodology to function. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 767-779 (2005).
87. De Benedictis, A. & Duffau, H. Brain hodotopy: from esoteric concept to practical surgical applications. Neurosurgery 68, 1709-1723 (2011).
88. Moritz-Gasser, S. & Duffau, H. Cognitive processes and neural basis of language switching: proposal of a new model. Neuroreport 20, 1577-1580 (2009).
89. Thiebaut de Schotten, M., Dell'Acqua, F., Valabregue, R. & Catani, M. Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48, 82-96 (2012).
90. Gil Robles, S., Gatignol, P., Capelle, L., Mitchell, M. C. & Duffau, H. The role of dominant striatum in language: a study using intraoperative electrical stimulations. J. Neurol. Neurosurg. Psychiatry 76, 940-946 (2005).
91. Teixidor, P. et al. Assessment of verbal working memory before and after surgery for low-grade glioma. J. Neurooncol. 81, 305-313 (2007).
92. Charras, P. et al. Functional reorganization of the attentional networks in low-grade glioma patients: a longitudinal study. Cortex 63, 27-41 (2014).
93. Fernández Coello, A. et al. Selection of intraoperative tasks for awake mapping based on relationships between tumor location and functional networks. J. Neurosurg. 119, 1380-1394 (2013).
94. Gatignol, P., Capelle, L., Le Bihan, R. & Duffau, H. Double dissociation between picture naming and comprehension: an electrostimulation study. Neuroreport 15, 191-195 (2004).
95. Plaza, M., Gatignol, P., Cohen, H., Berger, B. & Duffau, H. A discrete area within the left dorsolateral prefrontal cortex involved in visual-verbal incongruence judgment. Cereb. Cortex 18, 1253-1259 (2008).
96. Herbet, G. et al. Disrupting posterior cingulate connectivity disconnects consciousness from the external environment. Neuropsychologia 56, 239-244 (2014).
97. Duffau, H. Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol. 4, 476-486 (2005).
98. Duffau, H. Brain plasticity: from pathophysiological mechanisms to therapeutic applications. J. Clin. Neurosci. 13, 885-897 (2006).
99. Desmurget, M., Bonnetblanc, F. & Duffau, H. Contrasting acute and slow growing lesions: a new door to brain plasticity. Brain 130, 898-914 (2007).
100. Benzagmout, M., Gatignol, P. & Duffau, H. Resection of World Health Organization grade II gliomas involving Broca's area: methodological and functional considerations. Neurosurgery 61, 741-752 (2007).
101. Lubrano, V., Draper, L. & Roux, F. E. What makes surgical tumor resection feasible in Broca's area? Insights into intraoperative brain mapping. Neurosurgery 66, 868-875 (2010).
102. Tate, M. C., Herbet, G., Moritz-Gasser, S., Tate, J. E. & Duffau, H. Reply: Probabilistic map of language regions: challenge and implication. Brain 138, e338 (2015).
103. Sarubbo, S., Le Bars, E., Moritz-Gasser, S. & Duffau, H. Complete recovery after surgical resection of left Wernicke's area in awake patient: a brain stimulation and functional MRI study. Neurosurg. Rev. 35, 287-292 (2012).
104. Thiel, A. et al. Essential language function of the right hemisphere in brain tumor patients. Ann. Neurol. 57, 128-131 (2005).
105. Keidel, J. L., Welbourne, S. R. & Lambon Ralph, M. A. Solving the paradox of the equipotential and modular brain: a neurocomputational model of stroke vs. slow-growing glioma. Neuropsychologia 48, 1716-1724 (2010).
106. Papagno, C. et al. Connectivity constraints on cortical reorganization of neural circuits involved in object naming. Neuroimage 55, 1306-1313 (2011).
107. Duffau, H. Does post-lesional subcortical plasticity exist in the human brain? Neurosci. Res. 65, 131-135 (2009).
108. Duffau, H. Do brain tumours allow valid conclusions on the localisation of human brain functions? Cortex 47, 1016-1017 (2011).
109. De Witt Hamer, P. C., Robles, S. G., Zwinderman, A. H., Duffau, H. & Berger, M. S. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J. Clin. Oncol. 30, 2559-2565 (2012).
110. Duffau, H. & Mandonnet, E. The "onco-functional balance" in surgery for diffuse low-grade glioma: integrating the extent of resection with quality of life. Acta Neurochir. (Wien) 155, 951-957 (2013).
111. Duffau, H., Thiebaut de Schotten, M. & Mandonnet, E. White matter functional connectivity as an additional landmark for dominant temporal lobectomy. J. Neurol. Neurosurg. Psychiatry 79, 492-495 (2008).
112. Herbet, G., Lafargue, G., Bonnetblanc, F., Moritz-Gasser, S. & Duffau, H. Is the right frontal cortex really crucial in the mentalizing network? A longitudinal study in patients with a slow-growing lesion. Cortex 49, 2711-2727 (2013).
113. Duffau, H. Jazz improvisation, creativity and brain plasticity. World Neurosurg. 81, 508-510 (2014).
114. Mandonnet, E. & Duffau, H. Understanding entangled cerebral networks: a prerequisite for restoring brain function with brain-computer interfaces. Front. Syst. Neurosci. 8, 82 (2014).