In Vivo Identification of Thick, Thin, and Pale Stripes of Macaque Area V2 Using Submillimeter Resolution (f)MRI at 3 T

Abstract

Primate area V2 contains a repetitive pattern of thick, thin and pale cytochrome oxidase stripes that are characterized by largely discrete in- and output channels, as well as differences in function, and myelo- and cytoarchitecture. Stripes have been identified mainly using microscope-based imaging of tiny portions of superficially located V2, or by postmortem methods, hence, the quest for (quasi) noninvasive tools to study these mesoscale functional units. Only recently, stripe-like V2 patterns have been demonstrated in humans with high-field (functional) magnetic resonance imaging (f)MRI, but in both such studies only 2 stripe compartments could be identified. Although interstripe distances in monkeys are ~half of those in humans, we show that all 3 V2 stripe classes can be reliably separated using submillimeter (f)MRI (0.6 mm isotropic voxels) on regular 3 T scanners by combining contrast agents and implanted phased-array coils. Specifically, we show highly reproducible fMRI patterns, both within and across subjects, of color-selective thin and disparity-selective thick stripes. Furthermore, reliable MRI-based higher myelin-density was observed in pale stripes. Hence, this is the first study showing segregation of columns using (f)MRI-based methods in macaque cortex, which opens the possibility of studying these elementary building blocks of the visual system noninvasively on a large scale.

Asymmetries in Global Perception Are Represented in Near- versus Far-Preferring Clusters in Human Visual Cortex

“…Sensitivity to horizontal binocular disparity is one important cue for visual depth (i.e., visual distance from the observer). Disparity-sensitive (stereoselective) activity has been reported in multiple visual areas, including V2, V3, V3A, and V4, in electrophysiological and imaging studies in nonhuman primates (Adams and Zeki, 2001;Hinkle and Connor, 2001;Thomas et al, 2002;Watanabe et al, 2002;Tsao et al, 2003;Chen et al, 2008;Anzai et al, 2011;Li et al, 2019) and in neuroimaging studies in humans (Tsao et al, 2003;Neri et al, 2004;Goncalves et al, 2015;Nasr et al, 2016;Nasr and Tootell, 2018). In a previous study, by taking advantage of high-field, high-resolution neuroimaging techniques, we found that clusters of such disparity-selective neurons show a strong selectivity for low-SF visual components (Tootell and Nasr, 2017).…”

A new view of dorsal visual cortex in macaques revealed by submillimeter fMRI

“…For M3, the template was one EPI image acquired during the separate field map scanning session. Finally, a slice-by-slice undistortion correction was performed according to the template EPI using a B-spline grid-based nonlinear registration method to reduce frame-to-frame distortions (Li et al, 2017).…”

“…The same procedures as in our previous study (Li et al, 2017) were used to register each EPI template and the results in the same space to the reference anatomy of each subject. For M3, a distortion field was calculated based on the field map acquired in the same session as the EPI template and this was applied to the GLM results using FSL, thereby correcting for EPI distortions caused by magnetic field inhomogeneity.…”

“…This yielded high-resolution (0.6 mm isotropic voxels) maps, close in resolution to most microelectrode retinotopic mapping studies (0.3~0.5 mm in depth, but 0.8~1 mm between penetrations parallel to the cortex). Using this technique, we have reliably identified finely-organized, interdigitated V2 stripes in awake behaving macaques, with high intra-and inter-subject reproducibility (Li et al, 2017).…”

The Blind Men and the Elephant: The Quest for Open Data Repositories

“…Conceivably, a similar pipeline can be constructed for anesthetized monkey data, although this will prove more challenging for awake nonhuman primate imaging data. Another major challenge may arise when high-resolution mesoscale data become available (Li et al, 2017). In certain instances, such data will be acquired from restricted parts of the brain, hampering their (automatic) registration with template brains.…”