Ventral and dorsal pathways for language

Abstract

Built on an analogy between the visual and auditory systems, the following dual stream model for language processing was suggested recently: a dorsal stream is involved in mapping sound to articulation, and a ventral stream in mapping sound to meaning. The goal of the study presented here was to test the neuroanatomical basis of this model. Combining functional magnetic resonance imaging (fMRI) with a novel diffusion tensor imaging (DTI)-based tractography method we were able to identify the most probable anatomical pathways connecting brain regions activated during two prototypical language tasks. Sublexical repetition of speech is subserved by a dorsal pathway, connecting the superior temporal lobe and premotor cortices in the frontal lobe via the arcuate and superior longitudinal fascicle. In contrast, higher-level language comprehension is mediated by a ventral pathway connecting the middle temporal lobe and the ventrolateral prefrontal cortex via the extreme capsule. Thus, according to our findings, the function of the dorsal route, traditionally considered to be the major language pathway, is mainly restricted to sensory-motor mapping of sound to articulation, whereas linguistic processing of sound to meaning requires temporofrontal interaction transmitted via the ventral route.

Fig. 1.

fMRI results. Functional networks involved in (A) repetition (of pseudowords compared with words) and (B) comprehension (listening to normal sentences compared to meaningless pseudo sentences), analyzed in two random effects analyses (no. = 33). Activations are overlaid as maximum intensity projections (MIP; x, −70 to −20) on a canonical brain. Peak voxels within each cluster defined the nodes of the networks, which served as seed regions for the probabilistic fiber tracking. (C) Both contrasts (repetition, blue; comprehension, red) displayed along the x coordinate of the seed regions. Statistical threshold was set at P < 0.001, uncorrected. T1a/p, anterior/posterior superior temporal gyrus; T2a/p, anterior/posterior middle temporal gyrus; FUS, fusiform gyrus; F3orb/tri/op, pars orbitalis/triangularis and opercularis of the inferior frontal gyrus; FOP, deep frontal operculum; PMd, dorsal premotor cortex.

Fig. 2.

Fiber tracking results. Composite fiber networks subserving repetition (A) and comprehension (B) computed by averaging the pairwise connections of 33 subjects defined in the repetition and comprehension experiment, respectively. Three-dimensional tractography renderings visualize the spatial orientation of both networks. Crosshairs on sagittal sections indicate the orientation of the coronal and axial sections. Maximum PIBI (probability index forming part of the bundle of interest) values are given at the top of the color bar. EmC, extreme capsule; AF/SLF, arcuate and superior longitudinal fascicle; MdLF/ILF, middle and inferior longitudinal fascicle. Abbreviation of seed regions are as indicated in Fig. 1

Fig. 3.

Dual pathway network for language. Composite fiber network for repetition (blue) and comprehension (red). Three-dimensional tractography renderings visualize the spatial orientation of both networks to each other. Dashed white line illustrates the bisection of the frontal lobe into a ventral part, which is connected to the postrolandic brain via the ventral pathway and a dorsal part, which is connected to the postrolandic brain via the dorsal pathway. From peak voxels (indicated with an asterisk) within each pathway, mean PIBI values (y axis) were extracted to show the contribution of each temporofrontal connection to the respective pathway. On x axis, lower row indicates the temporal, upper row the frontal seed region of each pairwise connection. PIBI, probability index of forming part of the bundle of interest; PFC, prefrontal cortex; PMC, premotor cortex. Abbreviations of seed regions are as indicated in Fig. 1.