Variability of visual field maps in human early extrastriate cortex challenges the canonical model of organization of V2 and V3

Abstract

Visual field maps in human early extrastriate areas (V2 and V3) are traditionally thought to form mirror-image representations which surround the primary visual cortex (V1). According to this scheme, V2 and V3 form nearly symmetrical halves with respect to the calcarine sulcus, with the dorsal halves representing lower contralateral quadrants, and the ventral halves representing upper contralateral quadrants. This arrangement is considered to be consistent across individuals, and thus predictable with reasonable accuracy using templates. However, data that deviate from this expected pattern have been observed, but mainly treated as artifactual. Here, we systematically investigate individual variability in the visual field maps of human early visual cortex using the 7T Human Connectome Project (HCP) retinotopy dataset. Our results demonstrate substantial and principled inter-individual variability. Visual field representation in the dorsal portions of V2 and V3 was more variable than in their ventral counterparts, including substantial departures from the expected mirror-symmetrical patterns. In addition, left hemisphere retinotopic maps were more variable than those in the right hemisphere. Surprisingly, only one-third of individuals had maps that conformed to the expected pattern in the left hemisphere. Visual field sign analysis further revealed that in many individuals the area conventionally identified as dorsal V3 shows a discontinuity in the mirror-image representation of the retina, associated with a Y-shaped lower vertical representation. Our findings challenge the current view that inter-individual variability in early extrastriate cortex is negligible, and that the dorsal portions of V2 and V3 are roughly mirror images of their ventral counterparts.

Human Retinotopic Mapping: from Empirical to Computational Models of Retinotopy

“…If the retinotopic organization was similar across most individuals throughout the visual hierarchy, with small deviations and discontinuities seen as pure noise, then templatebased predictions could be more accurate than measurement (Benson et al, 2012;Dougherty et al, 2003). Evidence suggests, however, that there may be significant inter-individual variability in non-human primates (Angelucci & Rosa, 2015;Gattass et al, 1988;Zhu & Vanduffel, 2019) as well as in humans (Allen et al, 2021;Benson et al, 2014;Ribeiro et al, 2023;.…”

“…Two common features among the discussed optimization-based models are that they are 2-dimensional (flat) models of visual field maps in the visual cortex and assume a spatially consistent mapping based on a template. Therefore, these models do not accurately represent the geometry of the visual cortex as a convoluted cortical sheet in 3D space, as well as the evidence suggesting that there may be legitimate interindividual variability (Allen et al, 2021;Ribeiro et al, 2023;). An obvious conceptual addition to the literature would consider a learning mechanism for determining a mapping function capable of predicting retinotopy from anatomy without assuming a rigid topological template.…”

“…For example, it is often assumed that the dorsal third-tier visual cortex is occupied by a single continuous area (V3) that extends along the entire dorsal border of V2 (Benson et al, 2014;Wang et al, 2015, p. 20). However, research suggests that there may be a more complicated organization of the dorsal third-tier visual cortex in non-human primates (Angelucci & Rosa, 2015;Gattass et al, 1988;Sereno et al, 2015;Zhu & Vanduffel, 2019) and humans Ribeiro et al, 2023;. Furthermore, the unprecedented ability of deepRetinotopy to predict discontinuous representations of the lower vertical meridian at the anterior border of dorsal V3 suggests that this discontinuity is likely a real structure-related variation.…”

“…As we navigate the intricate landscape of the human visual cortex, consistent interindividual variability in functional organization across its expanse (Gao et al, 2022;Ribeiro et al, 2023;Zhen et al, 2015Zhen et al, , 2017 prompts new compelling questions:…”

“…The abundance of data at our disposal opens new avenues for understanding and modeling the retinotopic organization of the visual cortex. For example, the Human Connectome Project (HCP) 7T Retinotopy dataset has already been successfully leveraged in modeling individuallevel retinotopic organization Ribeiro et al, 2021) and was crucial to uncovering substantial variability in the retinotopic organization of human early visual areas (Ribeiro et al, 2023). Thus, we finish by discussing how these abundant data can be leveraged to further our understanding of the retinotopic organization of the human visual cortex.…”