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

Abstract

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.

Associative white matter connecting the dorsal and ventral posterior human cortex

“…Indeed, dMRI and tractography have been used to identify the gross anatomical features of major, canonical tracts, such as the SLF (Makris et al 2004;de Schotten et al 2011) , the Arc (Catani et al 2002Catani and Thiebaut de Schotten 2008) , the IFOF (Catani et al 2002;Wakana et al 2007;Catani and Thiebaut de Schotten 2008;Sarubbo et al 2013) or the ILF (Mori et al 2002;Catani et al 2002) . These modern investigations reproduce the earlier findings of conventional post mortem dissection methods (Mori et al 2005;Catani and de Schotten 2012;De Benedictis et al 2014;Mai et al 2015;Wang et al 2016;Sarubbo et al 2016) . We note that some discrepancies still exist between the description of white matter across primate species, in that some descriptions of the ILF, Arcuate, IFOF and MdLF might still be contentious Petrides and Pandya 2009;Forkel et al 2014;Takemura et al 2017) .…”

“…These canonical tracts include the superior longitudinal fasciculus (SLF), the arcuate fasciculus (Arc), the inferior longitudinal fasciculus (ILF), and the inferior fronto-occipital fasciculus (IFOF). Work using post mortem anatomical dissection continues to provide fundamental insights into the structure of these and other white matter tracts (De Benedictis et al 2014Wang et al 2016;Sarubbo et al 2016;Hau et al 2017) .…”

New insights in the homotopic and heterotopic connectivity of the frontal portion of the human corpus callosum revealed by microdissection and diffusion tractography

“…These fascicles subserve the dorsal phonological and the ventral semantic streams of language processing, respectively Martino et al, 2010Martino et al, , 2013. The high level of structural intersection between SLF and IFOF has been highlighted in previous studies, especially within the frontal region [De Benedictis et al, 2012Sarubbo et al, 2013Sarubbo et al, , 2016. This anatomical feature corresponds also to a strict functional integration, as revealed by direct stimulation data [Ius et al, 2011;Sarubbo et al, 2015a,b] and cortical fMRI analysis [Tate et al, 2014;Vigneau et al, 2006].…”

“…10 and 11). The high level of structural intersection between SLF and IFOF has been highlighted in previous studies, especially within the frontal region [De Benedictis et al, 2012Sarubbo et al, 2013Sarubbo et al, , 2016. The high level of structural intersection between SLF and IFOF has been highlighted in previous studies, especially within the frontal region [De Benedictis et al, 2012Sarubbo et al, 2013Sarubbo et al, , 2016.…”

Heschl’s gyrus fiber intersection area: a new insight on the connectivity of the auditory-language hub

“…All of the bundles of fibers with cortical terminations in Heschl's gyrus or crossing the subcortical area underneath were isolated, including the anterior segment of the arcuate fasciculus (A-Arc), the long segment of the arcuate fasciculus (L-Arc), the middle longitudinal fasciculus (MLF), the optic radiation (OR), the inferior fronto-occipital fasciculus (IFOF), and the acoustic radiation. The acoustic radiation was approached by starting the dissection from the posterior third of the superior temporal sulcus as described by Sarubbo et al, 23 whereas the rest of the fascicles (the A-Arc, MLF, OR, and IFOF) were dissected according to the method described previously by our group. 16…”