Linking individual differences in human primary visual cortex to contrast sensitivity around the visual field

Abstract

The size and organization of primary visual cortex (V1) varies across individuals. Across individuals, V1 size varies more than twofold. Within individuals, cortical magnification varies with eccentricity and polar angle. Contrast sensitivity has been hypothesized to be limited by cortical resources, and specifically by the number of activated V1 neurons. Here, we quantify the relation between contrast sensitivity and V1 cortical magnification as a function of both individual observers and polar angle. We measured contrast sensitivity at four polar angle meridians in 29 observers. We then used fMRI to measure the size of V1 in the same observers, and the amount of surface area representing the same four meridians as the contrast sensitivity measurements (wedge-ROIs within 15 deg of the meridians, extending from 1 to 8 deg eccentricity). We found that: First, average contrast sensitivity per observer (averaged across polar angles) was predicted by the overall size of V1. Second, contrast sensitivity at each polar angle location was correlated with the surface area of the wedge-ROIs centered at the corresponding meridian. Third, the increases for contrast sensitivity and cortical magnification at the horizontal compared to vertical meridian (horizontal-vertical anisotropy, 'HVA') were strongly correlated: a larger HVA in contrast sensitivity corresponded to a larger HVA in cortical magnification. These results reveal that contrast sensitivity and cortical magnification co-vary across observers and demonstrate a link between perceptual polar angle asymmetries and cortical anatomy. Broadly, the results show a link between visual perception and the idiosyncratic cortical organization of V1 of neurotypical observers.

Presaccadic attention enhances contrast sensitivity, but not at the upper vertical meridian

“…However, a computational observer model has shown that these retinal asymmetries only account for a small proportion of behavioral contrast sensitivity asymmetries ( Kupers et al., 2019 , 2022 ). These asymmetries also exist and are greatly amplified, in the distribution of cortical surface area in the primary visual cortex, where there is substantially less surface dedicated to processing the upper vertical meridian than the lower vertical meridian ( Benson et al., 2021 ; Himmelberg et al., 2021a , b ). Thus, there is a reduction in neural resources allocated to the upper vertical meridian that could likely explain poorer visual performance.…”

Cortical magnification eliminates differences in contrast sensitivity across but not around the visual field

“…Contrast sensitivity, a fundamental visual capability, declines across eccentricity 1 and varies with polar angle: sensitivity is higher along the horizontal than vertical meridian –HorizontalVertical Anisotropy (HVA)– and along the lower than upper vertical meridian –Vertical Meridian Asymmetry (VMA) 2–7 . Cortical magnification, the linear extent of cortex corresponding to one degree of visual angle (mm/°), declines with eccentricity 8 and links behavior to brain structure 9–12 (‘Quantitative’ hypothesis).…”

“…For fixed-size and M-scaled gratings, the VMA extent reached a maximum of 40% at 1 cpd in the parafovea and 8 cpd in the perifovea. The VMA had only been characterized at eccentricities >2° 2–4,6,7 . This near-foveal location reveals that the SF at which the VMA peaks depends on eccentricity.…”

“…Optical and retinal factors only partially explain higher sensitivity for the HM than VM (<20%) and even less for the LVM than UVM (<5%) 22 . Psychophysical measures of acuity 20,23 and contrast sensitivity 6,7 correlate with the >60% more striatal surface area for the HM than VM and >25% for the LVM than UVM 7,23 . However, compensating for striate-cortical magnification around the visual field did not equate contrast sensitivity.…”

Retinal ganglion cell endowment is correlated with optic tract fiber cross section, not density

“…It is possible that individual variation in the distribution (as opposed to overall quantity) of retinal cell populations over eccentricity or polar angle may be reflected in the visual cortex. Indeed, recent work has shown that polar angle variation in group and individual measures of perception are related to variation in cortical magnification across area V1 (Benson et al, 2021;Himmelberg, et al, 2021;Kupers et al, 2022).…”