Asymmetries in Global Perception Are Represented in Near- versus Far-Preferring Clusters in Human Visual Cortex

Abstract

Human perception is more "global" when stimuli are viewed within the lower (rather than the upper) visual field. This phenomenon is typically considered as a 2-D phenomenon, likely due to differential neural processing within dorsal versus ventral cortical areas that represent lower versus upper visual fields, respectively. Here we test a novel hypothesis that this vertical asymmetry in global processing is a 3-D phenomenon associated with (1) higher ecological relevance of low-spatial frequency (SF) components in encoding near (compared with far) visual objects and (2) the fact that near objects are more frequently found in lower rather than upper visual fields. Using high-resolution fMRI, collected within an ultra-high-field (7 T) scanner, we found that the extent of vertical asymmetry in global visual processing in human subjects (n ϭ 10) was correlated with the fMRI response evoked by disparity-varying stimuli in human cortical area V3A. We also found that near-preferring clusters in V3A, located within stereoselective cortical columns, responded more selectively than far-preferring clusters, to low-SF features. These findings support the hypothesis that vertical asymmetry in global processing is a 3-D (not a 2-D) phenomenon, associated with the function of the stereoselective columns within visual cortex, especially those located within visual area V3A.

Ultra-High-Field Neuroimaging Reveals Fine-Scale Processing for 3D Perception

“…Combining 7T imaging with MVPA, we demonstrate a role of dorsal areas (V3A, V7) in 3D perception, consistent with previous fMRI studies showing a) disparity-evoked fMRI responses in V1, V3A, and V7 ( Bridge and Parker, 2007 ; Preston et al, 2008 ; Goncalves et al, 2015 ; Rideaux and Welchman, 2019 ; Nasr and Tootell, 2020 ), b) discriminable multivoxel fMRI pattern responses to disparity-defined position (i.e., near vs. far planes) in V3A ( Preston et al, 2008 ; Goncalves et al, 2015 ; Patten and Welchman, 2015 ; Li et al, 2017 ; Liu et al, 2020 ). Our fMRI results extend beyond these previous studies by demonstrating layer-specific representations related to stereoscopic perception in V3A and V7 (i.e., higher MVPA accuracy for correlated than anti-correlated stimuli in upper than deeper layers).…”

“…Second, we demonstrate feedback connectivity specific to stereoscopic perception (i.e., stronger connectivity for correlated than anti-correlated stimuli) between deeper V1 and V3A layers, suggesting top-down influences to disparity processing in primary visual cortex through feedback from higher visual dorsal areas known to be involved in stereo vision and disparity ( Goncalves et al, 2015 ; Nasr and Tootell, 2020 ). Previous neurophysiology studies have shown attenuated responses in V1 for anti-correlated compared to correlated stimuli ( Cumming and Parker, 1997 ; also in circuit simulation: Samonds et al, 2013 ).…”

“…Human neuroimaging studies have revealed widespread responses to binocular signals in occipito-parietal regions ( Bridge and Parker, 2007 ; Welchman, 2016 ) with the strongest modulation of brain activity by binocular signals in areas V3A and V7 ( Backus et al, 2001 ; Tsao et al, 2003 ; Preston et al, 2008 ; Minini et al, 2010 ; Cottereau et al, 2011 ; Goncalves et al, 2015 ; Rideaux and Welchman, 2019 ; Liu et al, 2020 ). There is evidence for local clustering of disparity-selective organization in area V3A ( Goncalves et al, 2015 ; Parker et al, 2017 ; Tootell and Nasr, 2017 ; Nasr and Tootell, 2020 ), as well as V2 and V3 ( Nasr and Tootell, 2018 ). These findings indicate parts of the dorsal visual cortex that are heavily involved in processing disparity signals.…”

Seeing and Extrapolating motion trajectories share common informative activation patterns in primary visual cortex

“…However, this similarity in univariate activation patterns was less pronounced for the upper visual areas (lower visual field), rather an overall higher activation in upper V1 relative to lower V1 was observed regardless of visual trajectory. Asymmetry in the upper vs. lower visual quadrants has been previously reported and one possible explanation might be the distribution of ‘near-preferring’ neurons, which tend to be more frequent in lower VF compared to upper VF (Nasr & Tootell, 2018, 2020; Karim & Kojima, 2017). In general, psychophysiological studies demonstrated that lower visual field seems to be more thoroughly engaged in tasks from different domains, such as motion (Danckert & Goodale, 2001; Levine & McAnany, 2005, Lakha & Humphreys, 2005), colour discrimination and hue sensitivity (Levine & McAnany, 2005).…”

Co-fluctuations of neural activity define intra-V1 networks related to perceptual organization

“…Relatively lower SF components are critical for extracting the Global shape in Navon figures, whereas higher SF components play a more significant role in the perception of local shapes (Flevaris & Robertson, 2016). The neural basis of this vertical asymmetry has been recently examined (Nasr & Tootell, 2020).…”