Cortical magnification in human visual cortex parallels task performance around the visual field

Abstract

Human vision has striking radial asymmetries, with performance on many tasks varying sharply with stimulus polar angle. Performance is generally better on the horizontal than vertical meridian, and on the lower than upper vertical meridian, and these asymmetries decrease gradually with deviation from the vertical meridian. Here we report cortical magnification at a fine angular resolution around the visual field. This precision enables comparisons between cortical magnification and behavior, between cortical magnification and retinal cell densities, and between cortical magnification in twin pairs. We show that cortical magnification in human primary visual cortex, measured in 163 subjects, varies substantially around the visual field, with a pattern similar to behavior. These radial asymmetries in cortex are larger than those found in the retina, and they are correlated between monozygotic twin pairs. These findings indicate a tight link between cortical topography and behavior, and suggest that visual field asymmetries are partly heritable.

Severe distortion in the representation of foveal visual image locations in short term memory

“…Here, overrepresentation is schematized as smaller visual receptive fields (circles); note that lower visual field receptive fields are schematized as also being smaller than upper visual field receptive fields. Evidence for such visual field anisotropies exists (Benson et al, 2021;Krukowski & Stone, 2005;Silva et al, 2018;Van Essen et al, 1984) and is consistent with our observations. (B) With saccadic reporting, location readout might be more dependent on oculomotor maps, which can have very different anisotropies.…”

“…3 between the horizontal and vertical meridians), and they are in line with evidence that visual meridian performance differences in the periphery persist in short term memory tasks (Montaser-Kouhsari & Carrasco, 2009). In fact, our manual response results can also suggest that anisotropies in representing visual field locations in cortex (Benson et al, 2021;Silva et al, 2018;Van Essen et al, 1984) extend well into the smalleccentricity foveal representations, which makes sense given the large amount of neural tissue magnification associated with foveal eccentricities. In that regard, it is interesting that differences in perceptual (Appelle, 1972;Ball & Sekuler, 1987;Girshick, Landy, & Simoncelli, 2011;Heeley & Buchanan-Smith, 1992;Krukowski & Stone, 2005;Li et al, 2003;Tomassini, Morgan, & Solomon, 2010) and oculomotor (Krukowski & Stone, 2005) performance often demonstrate a so-called oblique effect, in which performance is worse at oblique directions.…”

“…For example, readout of a foveally magnified neural map (at different locations) should be similar whether there is a wide hill of activation (diffuse memory trace) versus a narrower hill of activation (which might result from actual stimulus onset). Rather, anisotropies in neural representations of the visual field, that go beyond foveal magnification, might be at play as well (Benson et al, 2021;Silva et al, 2018;Van Essen et al, 1984). Indeed, anisotropies in visual field representations also exist in brain areas relevant for oculomotor readout in our task, as exemplified by the large difference between how the superior colliculus represents the upper and lower visual fields (Hafed & Chen, 2016).…”

“…In the visual cortex, anisotropies are related to behavior (Benson et al, 2021;Chapman & Bonhoeffer, 1998;De Valois, Yund, & Hepler, 1982;Li, Peterson, & Freeman, 2003;Silva et al, 2018;Van Essen et al, 1984). For example, visual performance on the horizontal meridian in a variety of tasks is better than performance on the vertical meridian (Carrasco et al, 2001;Talgar & Carrasco, 2002) , and also better than performance at oblique locations (Ball & Sekuler, 1987;Heeley & Buchanan-Smith, 1992;Krukowski & Stone, 2005).…”

“…For example, visual performance along the horizontal and vertical retinotopic meridians is different (Carrasco, Talgar, & Cameron, 2001;Liu, Heeger, & Carrasco, 2006;Talgar & Carrasco, 2002), and this difference is maintained in tasks involving short term memory (Montaser-Kouhsari & Carrasco, 2009). The fact that such visual meridian effects may be related to tissue magnification in visual cortical areas (Benson, Kupers, Babot, Carrasco, & Winawer, 2021;Silva et al, 2018;Van Essen, Newsome, & Maunsell, 1984) might then suggest that other known distortions in short term memory tasks, such as foveal biases in remembering peripheral target locations (Kerzel, 2002;Sheth & Shimojo, 2001), may also be related to how visual space is represented in topographic maps. If remembering visual target locations depends on both how visual space is topographically represented as well as on how memory information is neurally maintained, then an important remaining open question is whether foveal visual locations are recalled veridically or not, given the normally very high acuity nature of foveal vision in humans.…”