Linking individual differences in human V1 to perception around the visual field

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 organization of V1 differs greatly across individuals. Here, we used fMRI and psychophysics in the same individuals to quantify individual differences in V1 cortical magnification and perceptual contrast sensitivity at the four polar angle meridians. Across individuals, the overall size of V1 and localized cortical magnification both positively correlated with contrast sensitivity. Moreover, increases in cortical magnification and contrast sensitivity at the horizontal compared to the vertical meridian were strongly correlated. These data reveal a tight link between cortical anatomy and visual perception at the level of individual observer and stimulus location.

Linking contrast sensitivity to cortical magnification in human primary visual cortex

ABSTRACTThe size and organization of primary visual cortex (V1) varies across individuals. Across neurotypical adults, V1 size varies more than twofold. Within individuals, surface area per unit of visual field – cortical magnification – varies with eccentricity and polar angle. Contrast sensitivity and cortical magnification covary with eccentricity, therefore it has been hypothesized that cortical magnification, specifically the number of activated V1 neurons, limits contrast sensitivity. Here, we quantify the relation between contrast sensitivity and V1 cortical magnification across observers and polar angle. We measured contrast sensitivity at four cardinal 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 each of the four meridians (wedge-ROIs within 15° polar angle of the meridians, 1 to 8° eccentricity). We found that: First, an observer’s contrast sensitivity (averaged across polar angles) was predicted by the size of V1. Second, contrast sensitivity at each cardinal meridian was correlated with the surface area of the wedge-ROIs centered at the corresponding meridian. Third, increases in 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 in neurotypical observers.SIGNIFICANCE STATEMENTContrast sensitivity is a fundamental property of the human visual system, which indexes the limits of what one can detect or discriminate – the window of visibility. Contrast sensitivity varies with stimulus location on the retina and across observers. These variations are not well understood. Using psychophysics and magnetic resonance imaging, we tested the hypothesis that contrast sensitivity depends on the amount of responsive tissue in primary visual cortex (V1). Individuals with greater contrast sensitivity had a larger V1. Further, within observers, variation in contrast sensitivity across polar angle locations matched the variation in V1 surface area representing those locations. These findings demonstrate a tight link between visual perception and cortical anatomy, both within and among people.

Cortical Magnification in Human Visual Cortex Parallels Task Performance around the Visual Field

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.

Emergence of local and global synaptic organization on cortical dendrites

Synaptic inputs on cortical dendrites are organized with remarkable subcellular precision at the micron level. This organization emerges during early postnatal development through patterned spontaneous activity and manifests both locally where nearby synapses are significantly correlated, and globally with distance to the soma. We propose a biophysically motivated synaptic plasticity model to dissect the mechanistic origins of this organization during development and elucidate synaptic clustering of different stimulus features in the adult. Our model captures local clustering of orientation in ferret and receptive field overlap in mouse visual cortex based on the receptive field diameter and the cortical magnification of visual space. Including action potential back-propagation explains branch clustering heterogeneity in the ferret and produces a global retinotopy gradient from soma to dendrite in the mouse. Therefore, by combining activity-dependent synaptic competition and species-specific receptive fields, our framework explains different aspects of synaptic organization regarding stimulus features and spatial scales.

Topographic numerosity maps cover subitizing and estimation ranges

Numerosity, the set size of a group of items, helps guide behaviour and decisions. Non-symbolic numerosities are represented by the approximate number system. However, distinct behavioural performance suggests that small numerosities, i.e. subitizing range, are implemented differently in the brain than larger numerosities. Prior work has shown that neural populations selectively responding (i.e. hemodynamic responses) to small numerosities are organized into a network of topographical maps. Here, we investigate how neural populations respond to large numerosities, well into the ANS. Using 7 T fMRI and biologically-inspired analyses, we found a network of neural populations tuned to both small and large numerosities organized within the same topographic maps. These results demonstrate a continuum of numerosity preferences that progressively cover both the subitizing range and beyond within the same numerosity map, suggesting a single neural mechanism. We hypothesize that differences in map properties, such as cortical magnification and tuning width, underlie known differences in behaviour.

Expansion and contraction of resource allocation in sensory bottlenecks

Topographic sensory representations often do not scale proportionally to the size of their input regions, with some expanded and others contracted. In vision, the foveal representation is magnified cortically, as are the fingertips in touch. What principles drive this allocation, and how should receptor density, e.g. the high innervation of the fovea or the fingertips, and stimulus statistics, e.g. the higher contact frequencies on the fingertips, contribute? Building on work in efficient coding, we address this problem using linear second-order models that maximize information transmission through decorrelation. We introduce a sensory bottleneck to impose constraints on resource allocation and derive the optimal neural allocation. We find that bottleneck width is a crucial factor in resource allocation, inducing either expansion or contraction. Both receptor density and stimulus statistics affect allocation and jointly determine convergence for wider bottlenecks. Furthermore, we show a close match between the predicted and empirical cortical allocations in a well-studied model system, the star-nosed mole. Overall, our results suggest that the strength of cortical magnification depends on resource limits.

Cross-dataset reproducibility of population receptive field (pRF) estimates and cortical magnification asymmetries

Population receptive field (pRF) models fit to fMRI data are used to non-invasively measure retinotopic maps in human visual cortex, and these maps are a fundamental component of visual neuroscience experiments. We examined the reproducibility of retinotopic maps across two datasets: a newly acquired retinotopy dataset from New York University (NYU) (n=44) and a public dataset from the Human Connectome Project (HCP) (n=181). Our goal was to assess the degree to which pRF properties are similar across datasets, despite substantial differences in their experimental protocols. The two datasets differ in stimulus design, participant pool, fMRI protocol, MRI field strength, and preprocessing pipelines. We assessed the cross-dataset reproducibility of the two datasets in terms of the similarity of vertex-wise pRF estimates and in terms of large-scale cortical magnification properties. Within V1, V2, V3, and hV4, the group-median NYU and HCP vertex-wise polar angle estimates were nearly identical. Both eccentricity and pRF size estimates were also strongly correlated between the two datasets, but with a slope different from 1; the eccentricity and pRF size estimates were systematically greater in the NYU data. Next, to compare large-scale map properties, we quantified two polar angle asymmetries in V1 cortical magnification previously identified in the HCP data. The prior work reported more cortical surface area representing the horizontal than vertical visual field meridian, and the lower than upper vertical visual field meridian. We confirm both of these results in the NYU dataset. Together, our findings show that the retinotopic properties of V1-hV4 can be reliably measured between two datasets, despite numerous differences in their experimental design. fMRI-derived retinotopic maps are reproducible because they rely on an explicit computational model that is grounded in physiological evidence of how visual receptive fields are organized, allowing one to quantitatively characterize the BOLD signal in terms of stimulus properties (i.e., location and size). The new NYU Retinotopy Dataset will serve as a useful benchmark for testing hypotheses about the organization of visual areas and for comparison to the HCP Retinotopy Dataset.

Variability of the Surface Area of the V1, V2, and V3 Maps in a Large Sample of Human Observers

How variable is the functionally-defined structure of early visual areas in human cortex and how much variability is shared between twins? Here we quantify individual differences in the best understood functionally-defined regions of cortex: V1, V2, V3. The Human Connectome Project includes retinotopic measurements from 181 subjects, most of whom are twins. We trained four "anatomists" to manually define V1-V3 using retinotopic features. These definitions were more accurate than automated anatomical templates and showed that surface areas for these maps varied more than three-fold across individuals. The cortical magnification function also differed substantially among individuals: the relative amount of cortex devoted to central vision varied by more than a factor of 2. Whereas our twin sample sizes were too small to make precise heritability estimates (50 monozygotic pairs, 34 dizygotic), they nonetheless reveal high correlations, consistent with strong effects of the combination of shared genes and environment on visual area size. In V1, intraclass correlations of surface area between twin pairs were 84% and 68% for monozygotic and dizygotic pairs, respectively. The correlations were also high for V2 (81%, 73%) and V3 (75%, 43%). A trend for higher monozygotic than dizygotic size correlations, as well as greater similarity in map properties amongst monozygotic twins, suggest that visual area size and topography are partly genetically determined. Collectively, these results comprise the most accurate account of individual variability in visual area structure to date, and provide a robust population benchmark against which new individuals and developmental and clinical populations can be compared.

Geometry and Geodesy on the Primary Visual Cortex as a Surface of Revolution

Biological mapping of the visual field from the eye retina to the primary visual cortex, also known as occipital area V1, is central to vision and eye movement phenomena and research. That mapping is critically dependent on the existence of cortical magnification factors. Once unfolded, V1 has a convex three-dimensional shape, which can be mathematically modeled as a surface of revolution embedded in three-dimensional Euclidean space. Thus, we solve the problem of differential geometry and geodesy for the mapping of the visual field to V1, involving both isotropic and non-isotropic cortical magnification factors of a most general form. We provide illustrations of our technique and results that apply to V1 surfaces with curve profiles relevant to vision research in general and to visual phenomena such as ‘crowding’ effects and eye movement guidance in particular. From a mathematical perspective, we also find intriguing and unexpected differential geometry properties of V1 surfaces, discovering that geodesic orbits have alternative prograde and retrograde characteristics, depending on the interplay between local curvature and global topology.