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

Abstract

A central question in neuroscience is how the organization of cortical maps relates to perception, for which human primary visual cortex (V1) is an ideal model system. V1 nonuniformly samples the retinal image, with greater cortical magnification (surface area per degree of visual field) at the fovea than periphery and at the horizontal than vertical meridian. Moreover, the size and cortical magnification of V1 varies greatly across individuals. Here, we used fMRI and psychophysics in the same observers to quantify individual differences in V1 cortical magnification and contrast sensitivity at the four polar angle meridians. Across observers, the overall size of V1 and localized cortical magnification positively correlated with contrast sensitivity. Moreover, greater cortical magnification and higher contrast sensitivity at the horizontal than the vertical meridian were strongly correlated. These data reveal a link between cortical anatomy and visual perception at the level of individual observer and stimulus location.

Comparing retinotopic maps of children and adults reveals a late-stage change in how V1 samples the visual field

“…Children had no difference in the amount of V1 surface area representing the lower and upper vertical meridians of the visual field. Conversely, adults had more V1 surface area representing the lower than upper vertical meridian, consistent with prior work (Benson et al, 2021a;Himmelberg et al, 2021Himmelberg et al, , 2022aSilva et al, 2018). These findings parallel recent psychophysical findings showing that children have an HVA but no VMA in visual performance (Carrasco et al, 2022), whereas adults have both (Abrams et al, 2012;Barbot et al, 2021;Carrasco et al, 2001;Greenwood et al, 2017;Hanning et al, 2022;Himmelberg et al, 2020).…”

“…For example, contrast sensitivity matures around 12 years of age [55][56][57][58] , and both vernier acuity 4,59 and visual-spatial integration 6 continue to improve until around 14 years of age. All three of these tasks are plausibly dependent on the quality of the V1 representation: V1 neurons are highly sensitive to contrast [60][61][62][63][64] and are likely to limit contrast sensitivity 19,65 ; vernier acuity depends on the positional information encoded by V1 neurons 66,67 ; and visual-spatial integration depends on local orientation information extracted and integrated by V1 neurons 68 . The late maturation of visual performance on these tasks may reflect developmental changes in the response properties of V1 neurons or how V1 output is used by downstream neurons -or visual field maps-in the service of perception.…”

“…The specific implementation of this analysis is described below and in prior work 18,19 and circumvents discontinuities in surface area that would arise if we had defined the wedge-ROIs using estimates of pRF centers alone 18,93 .…”

“…In adults, the polar angle asymmetries in visual performance are well matched to cortical magnification; there is more V1 tissue representing the horizontal than vertical meridian, and the lower than upper vertical meridian of the visual field (Benson et al, 2021a;Himmelberg et al, 2021Himmelberg et al, , 2022aSilva et al, 2018). These cortical polar angle asymmetries have not been quantified in children.…”

Non-neural factors influencing BOLD response magnitudes within individual subjects

“…It is conceivable that genuine neural activity differences may exist across the horizontal and vertical meridian locations in V1. For example, there is greater cortical magnification along the horizontal than vertical meridian (Silva et al, 2018b; Benson et al, 2021; Himmelberg et al, 2021; Himmelberg et al, 2022), and it is plausible that this might be accompanied by differences in the strength of neural responses.…”