Differential white matter connections to ventral and lateral occipito-temporal face-selective regions underlie differences in visual field coverage

Abstract

The human face-processing network can be divided along two distinct streams: ventral occipito-temporal cortex (VOTC) containing IOG-faces, pFus-faces, and mFus-faces, and lateral occipito-temporal cortex (LOTC) containing pSTS-faces and mSTS-faces. VOTC regions are thought to be involved in processing face identity, while LOTC regions are involved in processing dynamic aspects of faces. Despite these differences in function, the anatomical or computational origins driving these differences remain unknown. As face identification and dynamic perception rely primarily on foveal and peripheral vision, respectively, we hypothesized that white-matter connections from early visual cortex (EVC) to ventral face-selective regions would originate more foveally than connections to lateral regions. To test this, we scanned 23 participants using 3T functional MRI and diffusion MRI. We used a functional localizer to identify face-selective regions in each participant, which were used as seed regions to functionally define white matter tracts. Then we tested to which eccentricities in EVC these tracts connected. We found that lateral regions were connected to more peripheral eccentricities in EVC (pSTS-faces: mean±SE = 7.1°±1.1 °; mSTS-faces: 11.9°±1.2°) than ventral regions (IOG-faces: 2.9±0.4°; pFus-faces: 4.7±0.6°; mFus-faces: 6.0±0.6°, outliers removed), where endpoint distributions all peaked within the central 3° (Figure 1). We next tested if white matter connections contribute to visual field coverage in face-selective regions. We conducted a second experiment (N=13) in which we estimated population receptive fields using a retinotopic mapping experiment. Consistent with the connectivity patterns, visual field coverage in ventral regions was foveally-biased, while visual coverage in LOTC regions extended much further into the periphery (Figure 2). Together, these findings demonstrate that (i) the anatomical and functional segregation of face-selective regions into two streams has a structural foundation and (ii) that differential patterns of white-matter connections from EVC to face-selective regions contribute to the differential visual field coverage across processing streams.

Acknowledgement: This research was funded by the NSF Graduate Research Development Program (grant DGE-114747) and Ruth L. Kirschstein National Research Service Award (grant F31EY027201) to JG, and the NIH (grants 1ROI1EY02231801A1, 1RO1EY02391501A1) to KGS and training grant 5T32EY020485 supporting VN