Myelin densities in retinotopically defined dorsal visual areas of the macaque

Xiaolian Li,Qi Zhu,Wim Vanduffel

doi:10.1007/s00429-021-02363-z

Abstract

The visuotopic organization of dorsal visual cortex rostral to area V2 in primates has been a longstanding source of controversy. Using sub-millimeter phase-encoded retinotopic fMRI mapping, we recently provided evidence for a surprisingly similar visuotopic organization in dorsal visual cortex of macaques compared to previously published maps in New world monkeys (Zhu and Vanduffel, Proc Natl Acad Sci USA 116:2306–2311, 2019). Although individual quadrant representations could be robustly delineated in that study, their grouping into hemifield representations remains a major challenge. Here, we combined in-vivo high-resolution myelin density mapping based on MR imaging (400 µm isotropic resolution) with fine-grained retinotopic fMRI to quantitatively compare myelin densities across retinotopically defined visual areas in macaques. Complementing previously documented differences in populational receptive-field (pRF) size and visual field signs, myelin densities of both quadrants of the dorsolateral posterior area (DLP) and area V3A are significantly different compared to dorsal and ventral area V3. Moreover, no differences in myelin density were observed between the two matching quadrants belonging to areas DLP, V3A, V1, V2 and V4, respectively. This was not the case, however, for the dorsal and ventral quadrants of area V3, which showed significant differences in MR-defined myelin densities, corroborating evidence of previous myelin staining studies. Interestingly, the pRF sizes and visual field signs of both quadrant representations in V3 are not different. Although myelin density correlates with curvature and anticorrelates with cortical thickness when measured across the entire cortex, exactly as in humans, the myelin density results in the visual areas cannot be explained by variability in cortical thickness and curvature between these areas. The present myelin density results largely support our previous model to group the two quadrants of DLP and V3A, rather than grouping DLP- with V3v into a single area VLP, or V3d with V3A+ into DM.

Highlights

The primate visual system encompasses more than 30 distinct visual areas (Felleman and Van Essen 1991)
This contrasts sharply with only one upper field quadrant described in posterior dorsal visual cortex of the macaque monkey, which is typically assigned to area V3A (Fig. 1a)
This section corresponds to an area named the parietooccipital area (PO) (Lewis and van Essen 2000) or V6 (Gamberini et al 2015; Hadjidimitrakis et al 2019), which was not identified in our retinotopic experiment due to limited visual field coverage of the stimuli

Summary

Introduction

The primate visual system encompasses more than 30 distinct visual areas (Felleman and Van Essen 1991). The most prominent macaque model, which became textbook knowledge and served as the model for the layout of the human visual cortex, claims a single dorsal area V3 (V3d) stretching along the anterior border of dorsal area V2 (V2d) and representing at least the central 40° of the lower visual field (Fig. 1a) This simple but widely accepted model contrasts sharply with other models based on the functional topography observed in New World monkeys. Detailed research revealed that New World monkeys typically have a larger number of quadrant representations in dorsal visual cortex immediately rostral to V2d, even with multiple upper field quadrants within the swath of expected lower field representations (Fig. 1c) This contrasts sharply with only one upper field quadrant described in posterior dorsal visual cortex of the macaque monkey, which is typically assigned to area V3A (Fig. 1a)

Methods

Results

Conclusion