A cross-validated cytoarchitectonic atlas of the human ventral visual stream

Abstract

The human ventral visual stream consists of several areas that are considered processing stages essential for perception and recognition. A fundamental microanatomical feature differentiating areas is cytoarchitecture, which refers to the distribution, size, and density of cells across cortical layers. Because cytoarchitectonic structure is measured in 20-micron-thick histological slices of postmortem tissue, it is difficult to assess (a) how anatomically consistent these areas are across brains and (b) how they relate to brain parcellations obtained with prevalent neuroimaging methods, acquired at the millimeter and centimeter scale. Therefore, the goal of this study was to (a) generate a cross-validated cytoarchitectonic atlas of the human ventral visual stream on a whole brain template that is commonly used in neuroimaging studies and (b) to compare this atlas to a recently published retinotopic parcellation of visual cortex (Wang et al., 2014). To achieve this goal, we generated an atlas of eight cytoarchitectonic areas: four areas in the occipital lobe (hOc1-hOc4v) and four in the fusiform gyrus (FG1-FG4), then we tested how the different alignment techniques affect the accuracy of the resulting atlas. Results show that both cortex-based alignment (CBA) and nonlinear volumetric alignment (NVA) generate an atlas with better cross-validation performance than affine volumetric alignment (AVA). Additionally, CBA outperformed NVA in 6/8 of the cytoarchitectonic areas. Finally, the comparison of the cytoarchitectonic atlas to a retinotopic atlas shows a clear correspondence between cytoarchitectonic and retinotopic areas in the ventral visual stream. The successful performance of CBA suggests a coupling between cytoarchitectonic areas and macroanatomical landmarks in the human ventral visual stream, and furthermore, that this coupling can be utilized for generating an accurate group atlas. In addition, the coupling between cytoarchitecture and retinotopy highlights the potential use of this atlas in understanding how anatomical features contribute to brain function. We make this cytoarchitectonic atlas freely available in both BrainVoyager and FreeSurfer formats (http://vpnl.stanford.edu/vcAtlas). The availability of this atlas will enable future studies to link cytoarchitectonic organization to other parcellations of the human ventral visual stream with potential to advance the understanding of this pathway in typical and atypical populations.

Human visual cortex is organized along two genetically opposed hierarchical gradients with unique developmental and evolutionary origins

“…For example, areas composing the visual processing hierarchy have been identified in living brains using anatomical and functional magnetic resonance imaging [2][3][4][5][6] , as well as in postmortem brains based on cytoarchitecture [7][8][9][10][11][12][13] , myeloarchitecture 14,15 , and receptor architecture [16][17][18] . Interestingly, and contrary to classic findings [19][20][21][22] , recent research in human postmortem brains indicates a tight correspondence between cellular transitions of cytoarchitectonic areas and cortical folding across the visual hierarchy 13,[23][24][25] . Similarly, recent research also indicates a tight correspondence between functional regions and cortical folding across the visual hierarchy for early 26 , middle [27][28][29] , and late 23,24,30 visual regions.…”

“…For example, hOc3d and hOc3v are within the same subcluster and yet, are located centimeters apart in cortex. Likewise, hOc4v is located within the posterior transverse collateral sulcus in ventral occipitotemporal cortex 25 , while hOc4d is located within the transverse occipital sulcus on the lateral surface of the brain 10 , and yet, both areas are positioned produced from a clustering algorithm on expression levels from the two gene clusters. The ordering of cROIs along the x-axis in the dendrogram is meaningful, as it represents the distance from hOc1 at the level of dendrogram leaves.…”

“…While measuring the expression of genes across discrete regions of cortex in vivo is infeasible, recent advances in transcriptomics and brain mapping have resulted in public databases detailing the transcriptome across the human cortical surface 41,42 . Furthermore, previous work from our group has provided multimodal solutions for linking different types of data to one another across spatial scales -for instance, linking functional regions at a millimeter scale in individual living human brains to cytoarchitectonic organization at a micron scale in individual postmortem brains 25,30,43 .…”

Mapping face categorization in the human ventral occipitotemporal cortex with direct neural intracranial recordings

“…For instance, in the described study, the large sample of participants allowed to split the anterior fusiform gyrus from adjacent sulci. Moreover, thanks to large samples, future iEEG studies might be able to use VOTC cytoarchitectonic divisions that might more closely match functional organization of the cortex than divisions on the basis of macroanatomic landmarks …”

Novel childhood experience suggests eccentricity drives organization of human visual cortex

“…We then generated a group average probability map of the location of Pokémon on the FreeSurfer average brain and thresholded maps from these 10 experienced participants to only include vertices that were consistent across at least 30% of participants. This threshold has been employed in previous research and demonstrates the optimal point in Dice coefficients for predicting ROI location in human cortices 75,88 . Furthermore, the thresholding ensures that no one subject in particular can influence the group average ROI.…”