Role of Population Receptive Field Size in Complex Visual Dysfunctions

Abstract

The neuronal mechanism of visual agnosia and foveal crowding that underlies the behavioral symptoms of several classic neurodegenerative diseases, including impaired holistic perception, navigation, and reading, is still unclear. A better understanding of this mechanism is expected to lead to better treatment and rehabilitation.OBJECTIVE To use state-of-the-art neuroimaging protocols to assess a hypothesis that abnormal population receptive fields (pRF) in the visual cortex underlie high-order visual impairments.DESIGN, SETTING, AND PARTICIPANTS Between April 26 and November 21, 2016, patients and controls were recruited from the Hadassah-Hebrew University medical center in a cross-sectional manner. Six patients with posterior cortical atrophy (PCA) were approached and 1 was excluded because of an inability to perform the task. Participants underwent functional magnetic resonance imaging-based cortical visual field mapping and pRF evaluation and performed a masked repetition priming task to evaluate visuospatial perception along the eccentricity axis. The association between pRF sizes and behavioral impairments was assessed to evaluate the role of abnormal pRF sizes in impaired visual perception. Posterior cortical atrophy is a visual variant of Alzheimer disease that is characterized by progressive visual agnosia despite almost 20/20 visual acuity. Patients with PCA are rare but invaluable for studying visual processing abnormalities following neurodegeneration, as atrophy begins in visual cortices but initially spares other brain regions involved in memory and verbal communication.EXPOSURES Participants underwent a magnetic resonance imaging scan. MAIN OUTCOMES AND MEASURESPopulation receptive field sizes and their association with visual processing along the fovea-to-periphery gradient.RESULTS Five patients with PCA (4 men [80%]; mean [SEM] age, 62.9 [3.5] years) were compared with 8 age-matched controls (1 man [25%]; mean [SEM] age, 63.7 [3.7] years) and demonstrated an atypical pRF mapping that varied along the eccentricity axis, which presented as abnormally small peripheral and large foveal pRFs sizes. Abnormality was seen in V1 (peripheral, 4.4°and 5.5°; foveal, 5.5°and 4.5°in patients and controls, respectively; P < .05) as well as in higher visual regions, but not in intermediate ones. Behaviorally, an atypical fovea-to-periphery gradient in visual processing was found that correlated with their pRF properties (r = 0.8; P < .01 for the correlation between pRF and behavioral fovea-to-periphery slopes).CONCLUSIONS AND RELEVANCE High-order visuocognitive functions may depend on abnormalities in basic cortical characteristics. These results may fundamentally change approaches to rehabilitation in such conditions, emphasizing the potential of low-level visual interventions.

Convergence Along the Visual Hierarchy Is Altered in Posterior Cortical Atrophy

“…We recently applied the population receptive field model to find indications that simultanagnosia can be explained by smaller population receptive fields at high eccentricity. 11 Additionally, we found that foveal crowding may result from larger foveal population receptive fields. These effects occurred predominantly in V1, even though cortical atrophy mainly affects extrastriate visual areas.…”

“…Connective field modeling was recently used to try to expand our insights into perceptual phenomena and neuro-ophthalmological disorders. 8 , 20 – 25 Following our previous work, in which we used stimulus-referred population receptive field models in PCA patients, 11 here we attempted to use this novel imaging method to untangle unanswered questions. Briefly, the main finding in our previous work was that the foveal population receptive fields of PCA patients were larger than those of controls, whereas the peripheral population receptive fields were smaller.…”

“…Briefly, the main finding in our previous work was that the foveal population receptive fields of PCA patients were larger than those of controls, whereas the peripheral population receptive fields were smaller. 11 The puzzling part was that these alterations were more pronounced in early visual areas, although pathology and cortical atrophy generally characterize extrastriate visual areas in PCA patients. 26 – 35 Thus, we hypothesized that the observed population receptive field changes were a consequence of a disruption in the delicate balance between excitatory and inhibitory signals in V1 through impaired feedback influences.…”

“…Population receptive field and connective field models were generated using VISTASOFT (GitHub, https://github.com/vistalab/vistasoft ), according to Haak et al 9 and Gravel et al 10 After the population receptive fields were modeled, eccentricity and polar angle maps were derived from them and used to delineate the primary visual cortex (V1), V2d, V2v, V3d, V3v, human V4 (hV4), and object-associated (lateral–occipital, LO) and motion-associated (temporal–occipital, TO) areas, as described by de Best et al 11 The number of voxels representing the cortical surface area was compared between groups, with no significant differences being found between cohorts. For connective field modeling, the activity of a voxel in the target area (e.g., V2) was predicted by blood oxygen-level dependent (BOLD) activity in the cortical surface of the source area (e.g., V1), termed V1 to V2 connective fields, as described in detail in Haak et al 9 …”

“…Yet, these changes in basic cortical characteristics are clinically manifested as a grouping of high-order visuocognitive functions. 11 Herein, we have used state-of-the-art connective field modeling protocols to investigate how high-order visual impairment may result from altered intervisual area interactions.…”