Structural and functional integration between dorsal and ventral language streams as revealed by blunt dissection and direct electrical stimulation

被引:65
作者
Sarubbo, Silvio [1 ,2 ]
De Benedictis, Alessandro [3 ]
Merler, Stefano [4 ]
Mandonnet, Emmanuel [5 ]
Barbareschi, Mattia [6 ]
Dallabona, Monica [1 ]
Chioffi, Franco [1 ,2 ]
Duffau, Hugues [7 ,8 ]
机构
[1] Santa Chiara Hosp, Trento APSS, Dept Neurosci, Div Neurosurg, 9 Largo Medaglie Oro, I-38122 Trento, Italy
[2] Santa Chiara Hosp, Trento APSS, Struct & Funct Connect Lab, Div Neurosurg, 9 Largo Medaglie Oro, I-38122 Trento, Italy
[3] Bambino Gesu Pediat Hosp, IRCCS, Neurosurg Unit, Dept Neurosci & Neurorehabil, 4 Piazza St Onofrio, I-00165 Rome, Italy
[4] FBK, 18 Via Sommar, I-38123 Trento, Italy
[5] Hop Lariboisiere, Dept Neurosurg, 2 Rue Ambroise Pare, F-75010 Paris, France
[6] Santa Chiara Hosp, Trento APSS, Dept Histopathol, 9 Largo Medaglie Oro, I-38122 Trento, Italy
[7] Univ Montpellier, Med Ctr, Hop Gui De Chauliac, Dept Neurosurg, 80 Ave Augustin Fliche, F-34295 Montpellier, France
[8] St Eloi Hosp, Team Plast Cent Nervous Syst Stem Cells & Glial T, INSERM, Inst Neurosci Montpellier,U1051, Montpellier, France
关键词
language network; white matter; brain connectivity; blunt dissection; subcortical mapping; direct electrical stimulation; LONGITUDINAL FASCICULUS; ARCUATE FASCICLE; FIBER DISSECTION; SEMANTIC SYSTEM; NEURAL BASIS; BROCAS AREA; HUMAN BRAIN; CONNECTIVITY; PATHWAYS; INSIGHTS;
D O I
10.1002/hbm.23281
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
The most accepted framework of language processing includes a dorsal phonological and a ventral semantic pathway, connecting a wide network of distributed cortical hubs. However, the cortico-subcortical connectivity and the reciprocal anatomical relationships of this dual-stream system are not completely clarified. We performed an original blunt microdissection of 10 hemispheres with the exposition of locoregional short fibers and six long-range fascicles involved in language elaboration. Special attention was addressed to the analysis of termination sites and anatomical relationships between long- and short-range fascicles. We correlated these anatomical findings with a topographical analysis of 93 functional responses located at the terminal sites of the language bundles, collected by direct electrical stimulation in 108 right-handers. The locations of phonological and semantic paraphasias, verbal apraxia, speech arrest, pure anomia, and alexia were statistically analyzed, and the respective barycenters were computed in the MNI space. We found that terminations of main language bundles and functional responses have a wider distribution in respect to the classical definition of language territories. Our analysis showed that dorsal and ventral streams have a similar anatomical layer organization. These pathways are parallel and relatively segregated over their subcortical course while their terminal fibers are strictly overlapped at the cortical level. Finally, the anatomical features of the U-fibers suggested a role of locoregional integration between the phonological, semantic, and executive subnetworks of language, in particular within the inferoventral frontal lobe and the temporoparietal junction, which revealed to be the main criss-cross regions between the dorsal and ventral pathways. Hum Brain Mapp 37:3858-3872, 2016. (c) 2016 Wiley Periodicals, Inc.
引用
收藏
页码:3858 / 3872
页数:15
相关论文
共 91 条
[51]   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 [J].
Makris, N. ;
Preti, M. G. ;
Wassermann, D. ;
Rathi, Y. ;
Papadimitriou, G. M. ;
Yergatian, C. ;
Dickerson, B. C. ;
Shenton, M. E. ;
Kubicki, M. .
BRAIN IMAGING AND BEHAVIOR, 2013, 7 (03) :335-352
[52]   Evidence of a middle longitudinal fasciculus in the human brain from fiber dissection [J].
Maldonado, Igor Lima ;
de Champfleur, Nicolas Menjot ;
Velut, Stephane ;
Destrieux, Christophe ;
Zemmoura, Ilyess ;
Duffau, Hugues .
JOURNAL OF ANATOMY, 2013, 223 (01) :38-45
[53]   Cortex-sparing fiber dissection: an improved method for the study of white matter anatomy in the human brain [J].
Martino, Juan ;
Hamer, Philip C. De Witt ;
Vergani, Francesco ;
Brogna, Christian ;
Marco de Lucas, Enrique ;
Vazquez-Barquero, Alfonso ;
Garcia-Porrero, Juan A. ;
Duffau, Hugues .
JOURNAL OF ANATOMY, 2011, 219 (04) :531-541
[54]   Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study [J].
Martino, Juan ;
Hamer, Philip C. De Witt ;
Berger, Mitchel S. ;
Lawton, Michael T. ;
Arnold, Christine M. ;
Marco de Lucas, Enrique ;
Duffau, Hugues .
BRAIN STRUCTURE & FUNCTION, 2013, 218 (01) :105-121
[55]   Functional connectivity in the human language system:: a cortico-cortical evoked potential study [J].
Matsumoto, R ;
Nair, DR ;
LaPresto, E ;
Najm, I ;
Bingaman, W ;
Shibasaki, H ;
Lüders, HO .
BRAIN, 2004, 127 :2316-2330
[56]   Random local temporal structure of category fluency responses [J].
Meyer, David J. ;
Messer, Jason ;
Singh, Tanya ;
Thomas, Peter J. ;
Woyczynski, Wojbor A. ;
Kaye, Jeffrey ;
Lerner, Alan J. .
JOURNAL OF COMPUTATIONAL NEUROSCIENCE, 2012, 32 (02) :213-231
[57]  
Meynert T, 1868, BAU GROSSHIRNRINDE S
[58]   Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: A brain electrostimulation study [J].
Moritz-Gasser, Sylvie ;
Herbet, Guillaume ;
Duffau, Hugues .
NEUROPSYCHOLOGIA, 2013, 51 (10) :1814-1822
[59]   What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval [J].
Papagno, Costanza ;
Miracapillo, Christiano ;
Casarotti, Alessandra ;
Lauro, Leonor J. Romero ;
Castellano, Antonella ;
Falini, Andrea ;
Casaceli, Giuseppe ;
Fava, Enrica ;
Bello, Lorenzo .
BRAIN, 2011, 134 :405-414
[60]   A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading [J].
Price, Cathy J. .
NEUROIMAGE, 2012, 62 (02) :816-847