Dissociation and convergence of the dorsal and ventral visual working memory streams in the human prefrontal cortex

Abstract

Visual information is largely processed through two pathways in the primate brain: an object pathway from the primary visual cortex to the temporal cortex (ventral stream) and a spatial pathway to the parietal cortex (dorsal stream). Whether and to what extent dissociation exists in the human prefrontal cortex (PFC) has long been debated. We examined anatomical connections from functionally defined areas in the temporal and parietal cortices to the PFC, using noninvasive functional and diffusion-weighted magnetic resonance imaging. The right inferior frontal gyrus (IFG) received converging input from both streams, while the right superior frontal gyrus received input only from the dorsal stream. Interstream functional connectivity to the IFG was dynamically recruited only when both object and spatial information were processed. These results suggest that the human PFC receives dissociated and converging visual pathways, and that the right IFG region serves as an integrator of the two types of information.

Figure 1

Experimental design for functional imaging.

Figure 2

(Upper panel) Activation maps superimposed on a three-dimensional brain. Areas in green were active to spatial stimuli, while areas in red were active to face stimuli during the encoding phase. The image on the left side represents the right hemisphere, and includes all activated areas with a height threshold of p < 0.001 (uncorrected). Activated areas with a height threshold of p < 0.001, corrected for whole-brain multiple comparisons at the cluster level (p < 0.01), are listed in Table 1. (Lower panel) Group analyses (n = 15) of tractography from the right FG (A, B) and right IPS (C, D). Population maps (A, C) and BOOT-TRAC probabilistic maps (B, D) are superimposed on a T1-weighted template brain. Talairach coordinates of each section are shown on top of each panel. Red areas in the population maps (right FG in panel A, right IPS in panel C) represent activated areas in the right FG (A) and right IPS (C). The dark blue arrowheads point to areas around the right SFG, while light blue arrowheads point to areas around the right ventral IFG. See also Supplementary Table S1 and Table S2.

Figure 3

(A) Population maps of the dorsal and ventral pathways projected onto a three-dimensional template brain. Terminal points of tractography (n > 5) from the activated area in the right IPS are shown in green, and terminal points of tractography (n > 5) from the activated area in the right FG are shown in red. Overlap areas from the two pathways were shown in yellow. The dark blue arrowhead indicates the right SFG, and light blue arrowheads indicate the right ventral IFG. See also Supplementary Fig. S2. (B) Activation maps superimposed on a three-dimensional brain during the encoding (dark blue) and maintenance (light blue) phases of the combined condition. The image on the left side represents the right hemisphere, and includes all activated areas with a height threshold of p < 0.001 (uncorrected). The light blue arrowhead indicates the right ventral IFG.