A Whole-Brain Topographic Ontology

Abstract

It is a common view that the intricate array of specialized domains in the ventral visual pathway is innately prespecified. What this review postulates is that it is not. We explore the origins of domain specificity, hypothesizing that the adult brain emerges from an interplay between a domain-general map-based architecture, shaped by intrinsic mechanisms, and experience. We argue that the most fundamental innate organization of cortex in general, and not just the visual pathway, is a map-based topography that governs how the environment maps onto the brain, how brain areas interconnect, and ultimately, how the brain processes information.

Keywords: development; domain specificity; experience; topography.

Figure 1

Topographic organization of VTC. In cortical surface reconstructions of the human VTC, several organizing frameworks have been observed, including (a) retinotopy (Wang et al. 2015), (b) shape/curvature, (c) color, (d) object size, (e) animacy, and ( f ) distinct category-selective domains. Abbreviations: A, anterior; Ac, anterior color; Cc, central color; CoS, collateral sulcus; FFA, fusiform face area; hV4, human V4; IOG, inferior occipital gyrus; L, lateral; M, medial; OTS, occipitotemporal sulcus; P, posterior; Pc, posterior color; PCA, principal components analysis; PHC, parahippocampal cortex; PPA, parahippocampal place area; V, ventral; VO, ventral occipital; VTC, ventral temporal cortex. Panel b adapted with permission from Yue et al. (2020), panel c adapted from Lafer-Sousa et al. (2016) (CC BY 4.0), panels d and e adapted from Konkle & Caramazza (2013) (CC BY-NC-SA 3.0), and panel f adapted with permission from Grill-Spector & Weiner (2014).

Figure 2

Maps, scale, and hierarchy. The primate visual system contains a hierarchically organized series of retinotopic maps that are also organized by selectivity for scale and shape. (a) Map of responsiveness to polar angle stimuli in the opposite visual field. (b) Map of responsiveness to stimulus eccentricity in the opposite visual field. (c) Hierarchical organization of the neonatal visual system, inferred from pairwise correlations between seed areas in functional MRI (Arcaro & Livingstone 2017a). Abbreviations: A, anterior; CIP, caudal intraparietal; D, dorsal; DP, dorsal prelunate; FST, fundus of the superior temporal sulcus; IT, inferior temporal; LIP, lateral intraparietal; MST, medial superior temporal; MT, middle temporal; OTd, occipitotemporal dorsal; OTS, occipitotemporal sulcus; P, posterior; PIT, posterior inferior temporal; V, ventral. Figure adapted from Arcaro & Livingstone (2017a).

Figure 3

Activity-acting-on-maps hypothesis. (a) Topographic maps established before birth provide the scaffolding for individual- and species-specific experience-driven domain development. Colors in the visual pathway (to the left of the first dotted line) indicate eccentricity. Colors between the next set of dotted lines indicate tuning for auditory tonotopy. Colors between the next pair of dotted lines indicate somatomotor maps, as indicated on the monkey icon. Colors in the most anterior part of the map (the frontal eye fields) again indicate visual field eccentricity. Panel a adapted from Arcaro & Livingstone (2021). (b) Early visual experience acts on this intrinsic architecture to sculpt selectivity. (Clockwise from upper left) Early face looking behavior sculpts face domains (Arcaro et al. 2017) (photograph by A. Stubbs, provided by the Neural Correlate Society); face deprivation prevents the formation of face domains (Arcaro et al. 2017) (photograph provided by M. Livingstone); learning to read leads to the formation of text domains (Dehaene et al. 2010) (photograph by D. Livingstone); playing Pokémon produces Pokémon domains (Gomez et al. 2019) (photograph provided by J. Gomez); and symbol learning forms symbol domains in macaques (Srihasam et al. 2012) (photograph by M. Livingstone). (c) Various functionally specific domains in macaques (left) and humans (right) form as a consequence of experience acting on visual maps. (Left to right) Face domains are absent in monkeys who lack face experience (maps adapted from Arcaro & Livingstone 2021); symbol domains are present in monkeys who learn to distinguish human symbols (maps adapted from Srihasam et al. 2012); word and letter domains are present in humans who have learned to read (maps adapted with permission from Feng et al. 2022); Pokémon domains are found in humans who played Pokémon extensively as children (maps adapted with permission from Gomez et al. 2019).

Figure 4

Map formation. (a) Evolutionarily preserved patterning of developing cortex. Panel a adapted with permission from Krienen & Buckner (2020). (b) Distortions in (i) areal patterning and (ii) internal map topography from changes in molecular guidance expression. Panel b, subpanel i adapted from Ochi et al. (2022) (CC BY 4.0); panel b, subpanel ii adapted with permission from Cang et al. (2005a). (c) Alignment of external-world orientation of sensory inputs across modalities. Abbreviations: LGN, lateral geniculate nucleus; S1, primary somatosensory cortex; V1, primary visual cortex; VP, ventral posterior nucleus.

Figure 5

Mirror maps in visual and somatomotor cortices. (a) Red and blue indicate reversals in the topographic progression of visual space. Panel a adapted from Janssens et al. (2014) (CC BY-NC-SA 3.0). (b) Colors indicate the topographic progression of finger representations in several maps (p < 0.0001, uncorrected, for the digit representation with the largest beta value). Panel b adapted from Arcaro et al. (2019a). Abbreviations: A, anterior; D, dorsal; P, posterior; STS, superior temporal sulcus; V, ventral; V1–4, visual cortices.

Figure 6

Principles of cross-modal map alignment. (a) Illustration of map convergence across modalities and takeover of deprived modality by intact modality. (b) Alignment of semantic categories in human lateral occipitotemporal cortex across visual-to-auditory modalities. The smaller image differentiates visual (red) from auditory (blue) activations. The green line illustrates the boundary between modalities. Panel b adapted with permission from Popham et al. (2021). (c) Topographic connectivity in macaque prefrontal cortex. Colors indicate corresponding points in topographic mapping between prefrontal and association cortices (frontal, parietal, and temporal). Panel c adapted with permission from Xu et al. (2022). (d) Topographic correlations in human prefrontal cortex. Each map shows three seeds (red, green, blue) in adjacent parts of prefrontal cortex, with correspondingly colored connectivity in temporal and parietal cortices. Panel d adapted from Yeo et al. (2011). Abbreviations: DMPFC, dorsomedial prefrontal cortex; ORBINS, orbitofrontal and insular cortices; PMC, posteromedial cortex; PPC, posterior parietal cortex; TEMP, temporal cortex.