Abstract
The orientation of a large grating can be decoded from V1 functional magnetic resonance imaging (fMRI) data, even at low resolution (3-mm isotropic voxels). This finding has suggested that columnar-level neuronal information might be accessible to fMRI at 3T. However, orientation decodability might alternatively arise from global orientation-preference maps. Such global maps across V1 could result from bottom-up processing, if the preferences of V1 neurons were biased toward particular orientations (e.g., radial from fixation, or cardinal, i.e., vertical or horizontal). Global maps could also arise from local recurrent or top-down processing, reflecting pre-attentive perceptual grouping, attention spreading, or predictive coding of global form. Here we investigate whether fMRI orientation decoding with 2-mm voxels requires (a) globally coherent orientation stimuli and/or (b) global-scale patterns of V1 activity. We used opposite-orientation gratings (balanced about the cardinal orientations) and spirals (balanced about the radial orientation), along with novel patch-swapped variants of these stimuli. The two stimuli of a patch-swapped pair have opposite orientations everywhere (like their globally coherent parent stimuli). However, the two stimuli appear globally similar, a patchwork of opposite orientations. We find that all stimulus pairs are robustly decodable, demonstrating that fMRI orientation decoding does not require globally coherent orientation stimuli. Furthermore, decoding remained robust after spatial high-pass filtering for all stimuli, showing that fine-grained components of the fMRI patterns reflect visual orientations. Consistent with previous studies, we found evidence for global radial and vertical preference maps in V1. However, these were weak or absent for patch-swapped stimuli, suggesting that global preference maps depend on globally coherent orientations and might arise through recurrent or top-down processes related to the perception of global form.
Highlights
Visual orientation information is thought to be represented in fine-scale columnar preference patterns in early visual cortex
Global-form differences, are not necessary for two orientation stimuli to be discriminable from early visual functional magnetic resonance imaging (fMRI) patterns
While we found some evidence for a radial preference map for patchswapped gratings, this effect was about an order of magnitude smaller than for globally coherent gratings. (And even for globally coherent gratings, the global preference map constituted a very subtle modulation of the overall V1 response, as shown in Figure 4.) This suggests that global radial and vertical preference maps in V1 are subtle and might depend to some extent on the degree of global coherence of the stimulus
Summary
Visual orientation information is thought to be represented in fine-scale columnar preference patterns in early visual cortex. Orientation sensitivity of 3-mm fMRI voxels could result from subtle biases in each voxel’s sample of columnar selectivities (Haynes and Rees, 2005; Kamitani and Tong, 2005) This idea had a big impact because it suggests that standard-resolution fMRI in humans allows us to decode columnar-scale neuronal representations. If V1 has a radial-preference map, a grating will elicit stronger feed-forward activation in V1 patches representing visual field regions where the grating’s edges point toward fixation Both evidence for (Freeman et al, 2011) and against (Mannion et al, 2009; Seymour et al, 2010) this account has been provided by recent neuroimaging studies
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