Functional definitions of parietal areas in human and non-human primates

Abstract

Establishing homologies between cortical areas in animal models and humans lies at the heart of translational neuroscience, as it demonstrates how knowledge obtained from these models can be applied to the human brain. Here, we review progress in using parallel functional imaging to ascertain homologies between parietal areas of human and non-human primates, species sharing similar behavioural repertoires. The human homologues of several areas along monkey IPS involved in action planning and observation, such as AIP, LIP and CIP, as well as those of opercular areas (SII complex), have been defined. In addition, uniquely human areas, such as the tool-use area in left anterior supramarginal gyrus, have also been identified.

Keywords: action observation; action planning; fMRI; homology.

Figure 1.

Human PPC areas hypothetically homologous to areas in the lateral bank of monkey IPS. (a,b) Confidence ellipses of five areas (brown, phAIP; pink, DIPSA; green, DIPSM; dark blue, POIPS; light blue, VIPS) in posterior parts of (a) left and (b) right flattened hemispheres (folded view in inset). (c,d) Parietal areas in (c) monkey and (d) human relative to V1–3, V6, retrosplenial cortex (RSC), transverse occipital sulcus (TOS) area and possible monkey counterparts (mRSC, mTOS); modified from Vanduffel et al. [18]. LOP is synonymous with CIP; IPS, intraparietal sulcus; CS, central sulcus. Symbols in (a)—local maxima (LM) for grasping: circle: [19]; squares: [20] (yellow), [21] (red), [22] (black), [23] (green), [24] (pink); visuo-tactile: [25] (brown); and 3D hand orientation: [26] (blue). In (b)—stars: LM of human LIP using spatial attention (orange, [27]) or saccades (blue, [28]); diamonds: other saccade LM: [15] (light and dark green), [29] (orange and red), [16] (black) and [28] (light blue); triangles: proposed human VIP: [30] (yellow), [31] (red), [32], (pink), [33] (green), [34], (blue), [16] (brown). Last two LM: visuo-tactile, others optic flow. Putative VIP LM stretch over 40 mm in medio-lateral direction, putative LIP LM over 40 mm in rostro-caudal direction, preventing the computation of useful confidence ellipses.

Figure 2.

Parallel imaging of 2D and 3D shape sensitivity: (a,b) lateral bank of left monkey IPS (from [45]) (a) 3D shape-from-disparity, (b) 2D shape sensitivity; (c–e) left human IPS (from [46])—(c) 3D shape-from-disparity; (d) 2D shape sensitivity; (e) saccade sensitivity (dark hatching); colours: see text. In (a,b) white dotted lines indicate the AIP/LIP borders derived from the saccade-related activation.

Figure 3.

Anterior IPS regions on left flatmap: (a) voxels specific for observation of manipulative (red, phAIP) and interpersonal actions (green, dDIPSA); (b,d) dDIPSA (black outline) relative to local maxima of studies as indicated (b), and to myelin density peak near middle IPS (d). (a,b,d) Modified from Ferri et al. [54]. Dots in (a)—IPS3 (purple), 4 (light blue) and 5 (yellow) from Konen et al. [55]. Symbols in (b)—stars: centre of numerosity (yellow) and size (red) maps averaged over four subjects from [56,57]; other symbols: LM of [34] (red), [32] (yellow), [58] (black), [59] (green). (c) Parietal part of human-specific resting-state network (red to yellow voxels) compared with hIPS (black outline): from [60], and outline of left anterior SMG region specific for human tool use: from [61] (pink), [62] (yellow) compared with phAIP (brown). Black dot indicates LM of interaction execution/tool [63].

Figure 4.

Retinotopic organizations: human V7/V7A cluster homologue of monkey CIP. (a,b) Eccentricity and azimuth CIP maps in the monkey (from [69])—stars: central representation, dotted lines: horizontal meridians, dashed lines: vertical meridians. (c) Overlap between functional VIPS and retinotopic V7: the rostral part of VIPS probably corresponds to V7A; (d,e) eccentricity and azimuth maps of posterior right hemisphere of subject 1 (same as in fig. 1 of [67]) centred on the V7/V7A cluster. Purple lines: far eccentricity borders of clusters; black stars: central representation, full and stippled black lines: lower and upper vertical meridians, white stippled lines: horizontal meridians. Arrows indicate rostral C clusters (1, 2), eccentricity ridge rostral to the V7/V7A cluster (3), centre of V6 (4) and a retinotopic map potentially corresponding to monkey DP (5).

Figure 5.

Homologies of parietal opercular areas. (a) Somatotopy of monkey areas (from [75]); (b) flatmap of left operculum indicating the four opercular areas (white outlines) and the five PF areas (coloured outlines); (c) somatopic organization of OP1, OP3 and OP4 [75]; (d) response to electrical stimulation median nerve in OP areas (from [76]); (e,f) activation sites for observation of skin-displacing action (e) and their activity profiles (f) from Ferri et al. [54].