Cartography and connectomes

Abstract

The past 25 years have seen great progress in parcellating the cerebral cortex into a mosaic of many distinct areas in mice, monkeys, and humans. Quantitative studies of interareal connectivity have revealed unexpectedly many pathways and a wide range of connection strengths in mouse and macaque cortex. In humans, advances in analyzing "structural" and "functional" connectivity using powerful but indirect noninvasive neuroimaging methods are yielding intriguing insights about brain circuits, their variability across individuals, and their relationship to behavior.

Figure 1

Volume and surface representations of mouse, macaque, and human brains. Top row: Parasagittal slices of high-resolution T1w scans from 3 species. The mouse and macaque data are described in Van Essen (2002a,b). The human individual and group average (120 subjects) are from HCP scans acquired at high spatial resolution (0.7 mm) rather than the 1 mm isotropic voxels conventionally used, Lower panels: Surface reconstructions are shown as midthickness surfaces (all 3) and inflated surfaces (flatmaps for the mouse). Cortical lobes are colored on the mouse surfaces; cerebellar lobules are colored for all 3 species. The mouse surface includes the olfactory bulb. The HCP surface reconstructions benefitted from refinements to standard FreeSurfer processing (Glasser et al., 2013b; Glasser et al., 2013c). The human cerebellar surface is from the Colin individual MRI atlas (Van Essen, 2002b).

Figure 2

Parcellations of mouse, macaque, and human cortex. A. A 40-area parcellation of mouse cortex illustrated on a cytochrome-oxidase stained tangential section of flattened mouse cortex. (Reproduced, with permission, from Wang et al., 2012). B. A composite parcellation of macaque cortex (Van Essen et al., 2012a) showing 130 areas of neocortex and transitional cortex, based on architectonic schemes of Lewis and Van Essen (2000b), Ferry et al. (2000), and Paxinos et al., (2000) and displayed on the inflated F99 atlas surface. C. A composite parcellation of 52 cortical areas spanning ~1/3 of human neocortex, based on published architectonic and retinotopic maps and displayed on the inflated Conte69 atlas surface (Van Essen et al., 2012a).(Ferry et al., 2000; Paxinos et al., 2000; Lewis and Van Essen, 2000b)

Figure 3

Parcellated connectomes for the macaque and mouse. Left column: Top row: 91-area parcellation of Markov et al. (2012). Row 2: 29 injected areas with each injected area colored on a dot placed on the estimated injection site. Row 3: Connectivity profile for area V2 (31 inputs). Row 4: Connectivity profile for area 8L (87 inputs). B. The 29×91 macaque connectome based on retrograde tracer injections, with 1,615 pathways. Reproduced, with permission, from Markov et al. (2012). C. The mouse connectome is based on anterograde tracers and the 40 area parcellation shown in Fig. 2. Reproduced, with permission, from Wang et al. (2012).

Figure 4

Diffusion MRI and probabilistic tractography results in an individual HCP subject. A. Lateral view of the ‘gray/white’ surface, showing a seed location in the inferior frontal gyrus (IFG, blue dot). B. Probabilistic streamlines in white matter on a coronal slice that intersects the IFG seed point. C. Probabilistic trajectories from the IFG seed point viewed in a 3D volume. D. Structural connectivity from the IFG seed point (large green dot) viewed on the inflated cortical surface. Smaller green dots indicate the approximate centers of patches showing high structural connectivity with the seed point. Red arrow indicates a likely false positive patch in insular cortex. Adapted, with permission, from Van Essen et al., 2013).

Figure 5

Multimodal analysis of HCP data in individuals and group averages for functional connectivity, myelin maps, and task-fMRI. A: Maps of cortical shape (FreeSurfer ‘sulc’ map) in an individual (top row) and a group average (bottom row, subjects) after FreeSurfer shape-based registration. B: Functional connectivity maps from a seed (black spot, red arrow) in parietal cortex, with hotspots in two patches in prefrontal cortex (arrows). C: Myelin maps, demonstrating myelin hotspots at the parietal seed location, in the area MT+ complex, and in the frontal eye fields and a nearby prefrontal patch (arrows). D: task-fMRI activation when viewing expressive faces in the HCP Emotion task, with activation foci that overlap with the parietal and prefrontal foci from the preceding panels.

Figure 6

ICA-based analysis of group-average functional connectivity. A. Four ICA-based components (“nodes”) from an analysis of 120 HCP subjects, registered using multimodal surface matching (Robinson et al., 2013b; Smith et al., 2013b). Top row: node 7 in the bilateral face representation of somato-motor cortex. Row 2: node 36, in the left hemisphere hand representation. Black contours show boundaries of areas 4a, 4p. 3a, 3b, and 1 (Van Essen et al., 2012b). Bottom panels: node 24 (bilateral central V1, row 3) and node 3 (bilateral peripheral V1, V2, row 4). B. Functional connectivity matrix for a 98 × 98 ICA analysis of data from 131 HCP subjects. The full correlation is shown above the diagonal and the partial correlation below the diagonal. Adapted, with permission, from Smith et al. (2013b).