Structural and functional integration between dorsal and ventral language streams as revealed by blunt dissection and direct electrical stimulation.
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. © 2016 Wiley Periodicals, Inc.
Division of Neurosurgery, Department of Neurosciences, "S. Chiara" Hospital, Trento APSS - 9 Largo Medaglie D'Oro, Trento, 38122, Italy. silviosarubbo@gmail.com.|Structural and Functional Connectivity Lab, Division of Neurosurgery, "S. Chiara" Hospital, Trento APSS - 9 Largo Medaglie D'Oro, Trento, 38122, Italy. silviosarubbo@gmail.com.
Silvio
S
Sarubbo
Department of Neuroscience and Neurorehabilitation, Neurosurgery Unit, Bambino Gesù Children's Hospital - IRCCS, 4 Piazza Sant'Onofrio, Roma, 00165, Italy.
Alessandro
A
De Benedictis
Bruno Kessler Foundation (FBK), 18 via Sommarive, Trento, 38123, Italy.
Stefano
S
Merler
Department of Neurosurgery, Lariboisiere Hospital, 2 Rue Ambroise Pare, Paris, 75010, France.
Emmanuel
E
Mandonnet
Department of Histopathology, "S. Chiara" Hospital, Trento APSS - 9 Largo Medaglie D'Oro, Trento, 38122, Italy.
Mattia
M
Barbareschi
Division of Neurosurgery, Department of Neurosciences, "S. Chiara" Hospital, Trento APSS - 9 Largo Medaglie D'Oro, Trento, 38122, Italy.
Monica
M
Dallabona
Division of Neurosurgery, Department of Neurosciences, "S. Chiara" Hospital, Trento APSS - 9 Largo Medaglie D'Oro, Trento, 38122, Italy.|Structural and Functional Connectivity Lab, Division of Neurosurgery, "S. Chiara" Hospital, Trento APSS - 9 Largo Medaglie D'Oro, Trento, 38122, Italy.
Franco
F
Chioffi
Department of Neurosurgery, Hôpital Gui De Chauliac, Montpellier University Medical Center, 80 Av Augustin Fliche, Montpellier, 34295, France.|Institute for Neuroscience of Montpellier, INSERM U1051, Team "Plasticity of Central Nervous System, Stem Cells and Glial Tumors," Saint Eloi Hospital, Montpellier, France.
Hugues
H
Duffau
D001921:Brain / Q000033:anatomy & histology* / Q000502:physiology*; D001931:Brain Mapping / Q000379:methods; D016000:Cluster Analysis; D004558:Electric Stimulation; D006801:Humans; D021621:Imaging, Three-Dimensional; D007802:Language; D042282:Microdissection; D009434:Neural Pathways / Q000000981:diagnostic imaging / Q000502:physiology
blunt dissection; brain connectivity; direct electrical stimulation; language network; subcortical mapping; white matter