Damien J. Mannion

Orientation anisotropies in human visual cortex.

Representing the orientation of features in the visual image is a fundamental operation of the early cortical visual system. The nature of such representations can be informed by considering anisotropic distributions of response across the range of orientations. Here we used functional MRI to study modulations in the cortical activity elicited by observation of a sinusoidal grating that varied in orientation. We report a significant anisotropy in the measured blood-oxygen level-dependent activity within visual areas V1, V2, V3, and V3A/B in which horizontal orientations evoked a reduced response. These visual areas and hV4 showed a further anisotropy in which increased responses were observed for orientations that were radial to the point of fixation. We speculate that the anisotropies in cortical activity may be related to anisotropies in the prevalence and behavioral relevance of orientations in typical natural environments.

Discrimination of the local orientation structure of spiral Glass patterns early in human visual cortex.

The local orientation structure of a visual image is fundamental to the perception of spatial form. Reports of reliable orientation-selective modulations in the pattern of fMRI activity have demonstrated the potential for investigating the representation of orientation in the human visual cortex. Orientation-selective voxel responses could arise from anisotropies in the preferred orientations of pooled neurons due to the random sampling of the cortical surface. However, it is unclear whether orientation-selective voxel responses reflect biases in the underlying distribution of neuronal orientation preference, such as the demonstrated over-representation of radial orientations (those collinear with fixation). Here, we investigated whether stimuli balanced in their radial components could evoke orientation-selective biases in voxel activity. We attempted to discriminate the sense of spiral Glass patterns (opening anti-clockwise or clockwise), in which the local orientation structure was defined by the placement of paired dots at an orientation offset from the radial. We found that information within the spatial pattern of fMRI responses in each of V1, V2, V3, and V3A/B allowed discrimination of the spiral sense with accuracies significantly above chance. This result demonstrates that orientation-selective voxel responses can arise without the influence of a radial bias. Furthermore, the finding indicates the importance of the early visual areas in representing the local orientation structure for the perception of complex spatial form.

Combination of subcortical color channels in human visual cortex.

Mechanisms of color vision in cortex have not been as well characterized as those in sub-cortical areas, particularly in humans. We used fMRI in conjunction with univariate and multivariate (pattern) analysis to test for the initial transformation of sub-cortical inputs by human visual cortex. Subjects viewed each of two patterns modulating in color between orange-cyan or lime-magenta. We tested for higher order cortical representations of color capable of discriminating these stimuli, which were designed so that they could not be distinguished by the postulated L-M and S-(L + M) sub-cortical opponent channels. We found differences both in the average response and in the pattern of activity evoked by these two types of stimuli, across a range of early visual areas. This result implies that sub-cortical chromatic channels are recombined early in cortical processing to form novel representations of color. Our results also suggest a cortical bias for lime-magenta over orange-cyan stimuli, when they are matched for cone contrast and the response they would elicit in the L-M and S-(L + M) opponent channels.

The influence of global form on local orientation anisotropies in human visual cortex.

Perception of the spatial structure of the environment results from visual system processes which integrate local information to produce global percepts. Here, we investigated whether particular global spatial arrangements evoke greater responses in the human visual system, and how such anisotropies relate to those evident in the responses to the local elements that comprise the global form. We presented observers with Glass patterns; images composed of randomly positioned dot pairings (dipoles) spatially arranged to produce a percept of translational or polar global form. We used functional magnetic resonance imaging (fMRI) to infer the magnitude of neural activity within early retinotopic regions of visual cortex (V1, V2, V3, V3A/B, and hV4) while the angular arrangement of the dipoles was modulated over time to sample the range of orientations. For both translational and polar Glass patterns, V1 showed an increased response to vertical dipole orientations and all visual areas showed a bias towards dipole orientations that were radial to the point of fixation. However, areas V1, V2, V3, and hV4 also demonstrated a bias, only present for polar Glass patterns, towards dipole orientations that were tangential to the point of fixation. This enhanced response to tangential orientations within polar form indicates sensitivity to curvature or more global form characteristics as early as primary visual cortex.

Color responsiveness argues against a dorsal component of human V4

The retinotopic organization, position, and functional responsiveness of some early visual cortical areas in human and non-human primates are consistent with their being homologous structures. The organization of other areas remains controversial. A critical debate concerns the potential human homologue of macaque area V4, an area very responsive to colored images: specifically, whether human V4 is divided between ventral and dorsal components, as in the macaque, or whether human V4 is confined to one ventral area. We used fMRI to define these areas retinotopically in human and to test the impact of image color on their responsivity. We found a robust preference for full-color movie segments over a luminance-matched achromatic version in ventral V4 but little or no preference in the vicinity of the putative dorsal counterpart. Contrary to previous reports that visual field coverage in the ventral part of V4 is deficient without the dorsal part, we found that coverage in ventral V4 extended to the lower vertical meridian, including the entire contralateral hemifield. Together these results provide evidence against a dorsal component of human V4. Instead, they are consistent with human V4 being a single, ventral region that is sensitive to the chromatic components of images.

Orientation-selective chromatic mechanisms in human visual cortex.

We used functional magnetic resonance imaging (fMRI) at 3T in human participants to trace the chromatic selectivity of orientation processing through functionally defined regions of visual cortex. Our aim was to identify mechanisms that respond to chromatically defined orientation and to establish whether they are tuned specifically to color or operate in an essentially cue-invariant manner. Using an annular test region surrounded inside and out by an inducing stimulus, we found evidence of sensitivity to orientation defined by red-green (L-M) or blue-yellow (S-cone isolating) chromatic modulations across retinotopic visual cortex and of joint selectivity for color and orientation. The likely mechanisms underlying this selectivity are discussed in terms of orientation-specific lateral interactions and spatial summation within the receptive field.

Consequences of polar form coherence for fMRI responses in human visual cortex

Relevant features in the visual image are often spatially extensive and have complex orientation structure. Our perceptual sensitivity to such spatial form is demonstrated by polar Glass patterns, in which an array of randomly-positioned dot pairs that are each aligned with a particular polar displacement (rotation, for example) yield a salient impression of spatial structure. Such patterns are typically considered to be processed in two main stages: local spatial filtering in low-level visual cortex followed by spatial pooling and complex form selectivity in mid-level visual cortex. However, it remains unclear both whether reciprocal interactions within the cortical hierarchy are involved in polar Glass pattern processing and which mid-level areas identify and communicate polar Glass pattern structure. Here, we used functional magnetic resonance imaging (fMRI) at 7T to infer the magnitude of neural response within human low-level and mid-level visual cortex to polar Glass patterns of varying coherence (proportion of signal elements). The activity within low-level visual areas V1 and V2 was not significantly modulated by polar Glass pattern coherence, while the low-level area V3, dorsal and ventral mid-level areas, and the human MT complex each showed a positive linear coherence response functions. The cortical processing of polar Glass patterns thus appears to involve primarily feedforward communication of local signals from V1 and V2, with initial polar form selectivity reached in V3 and distributed to multiple pathways in mid-level visual cortex.

Cortical and behavioral sensitivity to eccentric polar form

Patterns composed of local features aligned relative to polar angle, yielding starbursts, concentric circles, and spirals, can inform the understanding of spatial form perception. Previous studies have shown that starburst and concentric form instantiated in Glass patterns are, relative to spirals, both more readily detected in noise and evoke higher levels of blood-oxygen level-dependent (BOLD) signal, as measured with functional magnetic resonance imaging (fMRI), in the retinotopic cortex. However, such studies have typically presented the polar form at the center of gaze, which confounds the distribution of local orientations relative to fixation with variations in polar form. Here, we measure psychophysical detection thresholds and evoked BOLD signal to Glass patterns of varying polar orientation centered at eccentricity. We find an enhanced behavioral sensitivity to starburst and concentric form, consistent with previous studies. While visual areas V1, V2, V3, V3A/B, and hV4 showed elevated levels of BOLD activity to concentric patterns, V1 and V2 showed little to none of the increased activity to starburst patterns evident in areas V3, V3A/B, and hV4. Such findings demonstrate the anisotropic response of the human visual system to variations in polar form independent of variations in local orientation distributions.

Gain control in the response of human visual cortex to plaids

A recent intrinsic signal optical imaging study in tree shrew showed, surprisingly, that the population response of V1 to plaid patterns comprising grating components of equal contrast is predicted by the average of the responses to the individual components (MacEvoy SP, Tucker TR, Fitzpatrick D. Nat Neurosci 12: 637-645, 2009). This prompted us to compare responses to plaids and gratings in human visual cortex as a function of contrast and orientation. We found that the functional MRI (fMRI) blood oxygenation level-dependent (BOLD) responses of areas V1-V3 to a plaid comprising superposed grating components of equal contrast are significantly higher than the responses to a single component. Furthermore, the orientation response profile of a plaid is poorly predicted from a linear combination of the responses to its components. Together, these results indicate that the model of MacEvoy et al. (2009) cannot, without modification, account for the fMRI BOLD response to plaids in human visual cortex.

Orientation decoding: Sense in spirals?

The orientation of a visual stimulus can be successfully decoded from the multivariate pattern of fMRI activity in human visual cortex. Whether this capacity requires coarse-scale orientation biases is controversial. We and others have advocated the use of spiral stimuli to eliminate a potential coarse-scale bias-the radial bias toward local orientations that are collinear with the centre of gaze-and hence narrow down the potential coarse-scale biases that could contribute to orientation decoding. The usefulness of this strategy is challenged by the computational simulations of Carlson (2014), who reported the ability to successfully decode spirals of opposite sense (opening clockwise or counter-clockwise) from the pooled output of purportedly unbiased orientation filters. Here, we elaborate the mathematical relationship between spirals of opposite sense to confirm that they cannot be discriminated on the basis of the pooled output of unbiased or radially biased orientation filters. We then demonstrate that Carlsons (2014) reported decoding ability is consistent with the presence of inadvertent biases in the set of orientation filters; biases introduced by their digital implementation and unrelated to the brains processing of orientation. These analyses demonstrate that spirals must be processed with an orientation bias other than the radial bias for successful decoding of spiral sense.