The Emergence of Tuning to Global Shape Properties of Radial Frequency Patterns in the Ventral Visual Pathway.

Radial frequency (RF) patterns, created by sinusoidal modulations of a circle's radius, are processed globally when RF is low. These closed shapes therefore offer a useful way to interrogate the human visual system for global processing of curvature. RF patterns elicit greater responses than those to radial gratings in V4 and more anterior face-selective regions of the ventral visual pathway. This is largely consistent with work on nonhuman primates showing curvature processing emerges in V4, but is evident also higher up the ventral visual stream. Rather than contrasting RF patterns with other stimuli, we presented them at varied frequencies in a regimen that allowed tunings to RF to be derived from 8 human participants (3 female). We found tuning to low RF in lateral occipital areas and to some extent in V4. In a control experiment, we added a high-frequency ripple to the stimuli disrupting the local contour. Low-frequency tuning to these stimuli remained in the ventral visual stream, underscoring its role in global processing of shape curvature. We then used representational similarity analysis to show that, in lateral occipital areas, the neural representation was related to stimulus similarity, when it was computed with a model that captured how stimuli are perceived. We therefore show that global processing of shape curvature emerges in the ventral visual stream as early as V4, but is found more strongly in lateral occipital regions, which exhibit responses and representations that relate well to perception.SIGNIFICANCE STATEMENT We show that tuning to low radial frequencies, known to engage global shape processing mechanisms, was localized to lateral occipital regions. When low-level stimulus properties were accounted for such tuning emerged in V4 and LO2 in addition to the object-selective region LO. We also documented representations of global shape properties in lateral occipital regions, and these representations were predicted well by a proxy of the perceptual difference between the stimuli.

Temporal tuning of repetition suppression across the visual cortex.

The visual system adapts to its recent history. A phenomenon related to this is repetition suppression (RS), a reduction in neural responses to repeated compared with nonrepeated visual input. An intriguing hypothesis is that the timescale over which RS occurs across the visual hierarchy is tuned to the temporal statistics of visual input features, which change rapidly in low-level areas but are more stable in higher level areas. Here, we tested this hypothesis by studying the influence of the temporal lag between successive visual stimuli on RS throughout the visual system using functional (f)MRI. Twelve human volunteers engaged in four fMRI sessions in which we characterized the blood oxygen level-dependent response to pairs of repeated and nonrepeated natural images with interstimulus intervals (ISI) ranging from 50 to 1,000 ms to quantify the temporal tuning of RS along the posterior-anterior axis of the visual system. As expected, RS was maximal for short ISIs and decayed with increasing ISI. Crucially, however, and against our hypothesis, RS decayed at a similar rate in early and late visual areas. This finding challenges the prevailing view that the timescale of RS increases along the posterior-anterior axis of the visual system and suggests that RS is not tuned to temporal input regularities.NEW & NOTEWORTHY Visual areas show reduced neural responses to repeated compared with nonrepeated visual input, a phenomenon termed repetition suppression (RS). Here we show that RS decays at a similar rate in low- and high-level visual areas, suggesting that the short-term decay of RS across the visual hierarchy is not tuned to temporal input regularities. This may limit the specificity with which the mechanisms underlying RS could optimize the processing of input features across the visual hierarchy.

Laminar fMRI: Applications for cognitive neuroscience.

The cortex is a massively recurrent network, characterized by feedforward and feedback connections between brain areas as well as lateral connections within an area. Feedforward, horizontal and feedback responses largely activate separate layers of a cortical unit, meaning they can be dissociated by lamina-resolved neurophysiological techniques. Such techniques are invasive and are therefore rarely used in humans. However, recent developments in high spatial resolution fMRI allow for non-invasive, in vivo measurements of brain responses specific to separate cortical layers. This provides an important opportunity to dissociate between feedforward and feedback brain responses, and investigate communication between brain areas at a more fine- grained level than previously possible in the human species. In this review, we highlight recent studies that successfully used laminar fMRI to isolate layer-specific feedback responses in human sensory cortex. In addition, we review several areas of cognitive neuroscience that stand to benefit from this new technological development, highlighting contemporary hypotheses that yield testable predictions for laminar fMRI. We hope to encourage researchers with the opportunity to embrace this development in fMRI research, as we expect that many future advancements in our current understanding of human brain function will be gained from measuring lamina-specific brain responses.

Emergence of symmetry selectivity in the visual areas of the human brain: fMRI responses to symmetry presented in both frontoparallel and slanted planes.

Symmetry is effortlessly perceived by humans across changes in viewing geometry. Here, we re-examined the network subserving symmetry processing in the context of up-to-date retinotopic definitions of visual areas. Responses in object selective cortex, as defined by functional localizers, were also examined. We further examined responses to both frontoparallel and slanted symmetry while manipulating attention both toward and away from symmetry. Symmetry-specific responses first emerge in V3 and continue across all downstream areas examined. Of the retinotopic areas, ventral occipital VO1 showed the strongest symmetry response, which was similar in magnitude to the responses observed in object selective cortex. Neural responses were found to increase with both the coherence and folds of symmetry. Compared to passive viewing, drawing attention to symmetry generally increased neural responses and the correspondence of these neural responses with psychophysical performance. Examining symmetry on the slanted plane found responses to again emerge in V3, continue through downstream visual cortex, and be strongest in VO1 and LOB. Both slanted and frontoparallel symmetry evoked similar activity when participants performed a symmetry-related task. However, when a symmetry-unrelated task was performed, fMRI responses to slanted symmetry were reduced relative to their frontoparallel counterparts. These task-related changes provide a neural signature that suggests slant has to be computed ahead of symmetry being appropriately extracted, known as the "normalization" account of symmetry processing. Specifically, our results suggest that normalization occurs naturally when attention is directed toward symmetry and orientation, but becomes interrupted when attention is directed away from these features.

Multivariate Patterns in the Human Object-Processing Pathway Reveal a Shift from Retinotopic to Shape Curvature Representations in Lateral Occipital Areas, LO-1 and LO-2.

UNLABELLED: Representations in early visual areas are organized on the basis of retinotopy, but this organizational principle appears to lose prominence in the extrastriate cortex. Nevertheless, an extrastriate region, such as the shape-selective lateral occipital cortex (LO), must still base its activation on the responses from earlier retinotopic visual areas, implying that a transition from retinotopic to "functional" organizations should exist. We hypothesized that such a transition may lie in LO-1 or LO-2, two visual areas lying between retinotopically defined V3d and functionally defined LO. Using a rapid event-related fMRI paradigm, we measured neural similarity in 12 human participants between pairs of stimuli differing along dimensions of shape exemplar and shape complexity within both retinotopically and functionally defined visual areas. These neural similarity measures were then compared with low-level and more abstract (curvature-based) measures of stimulus similarity. We found that low-level, but not abstract, stimulus measures predicted V1-V3 responses, whereas the converse was true for LO, a double dissociation. Critically, abstract stimulus measures were most predictive of responses within LO-2, akin to LO, whereas both low-level and abstract measures were predictive for responses within LO-1, perhaps indicating a transitional point between those two organizational principles. Similar transitions to abstract representations were not observed in the more ventral stream passing through V4 and VO-1/2. The transition we observed in LO-1 and LO-2 demonstrates that a more "abstracted" representation, typically considered the preserve of "category-selective" extrastriate cortex, can nevertheless emerge in retinotopic regions. SIGNIFICANCE STATEMENT: Visual areas are typically identified either through retinotopy (e.g., V1-V3) or from functional selectivity [e.g., shape-selective lateral occipital complex (LOC)]. We combined these approaches to explore the nature of shape representations through the visual hierarchy. Two different representations emerged: the first reflected low-level shape properties (dependent on the spatial layout of the shape outline), whereas the second captured more abstract curvature-related shape features. Critically, early visual cortex represented low-level information but this diminished in the extrastriate cortex (LO-1/LO-2/LOC), in which the abstract representation emerged. Therefore, this work further elucidates the nature of shape representations in the LOC, provides insight into how those representations emerge from early retinotopic cortex, and crucially demonstrates that retinotopically tuned regions (LO-1/LO-2) are not necessarily constrained to retinotopic representations.

Global shape aftereffects in composite radial frequency patterns.

Individual radial frequency (RF) patterns are generated by modulating a circle's radius as a sinusoidal function of polar angle and have been shown to tap into global shape processing mechanisms. Composite RF patterns can reproduce the complex outlines of natural shapes and examining these stimuli may allow us to interrogate global shape mechanisms that are recruited in biologically relevant tasks. We present evidence for a global shape aftereffect in a composite RF pattern stimulus comprising two RF components. Manipulations of the shape, location, size and spatial frequency of the stimuli revealed that this aftereffect could only be explained by the attenuation of intermediate-level global shape mechanisms. The tuning of the aftereffect to test stimulus size also revealed two mechanisms underlying the aftereffect; one that was tuned to size and one that was invariant. Finally, we show that these shape mechanisms may encode some RF information. However, the RF encoding we found was not capable of explaining the full extent of the aftereffect, indicating that encoding of other shape features such as curvature are also important in global shape processing.

Brighter Time: A Smartphone App Recording Cognitive Task Performance and Illuminance in Everyday Life.

Light is an influential regulator of behavioural and physiological state in mammals. Features of cognitive performance such as memory, vigilance and alertness can be altered by bright light exposure under laboratory and field conditions. However, the importance of light as a regulator of performance in everyday life is hard to assess and has so far remained largely unclear. We set out to address this uncertainty by developing a tool to capture measures of cognitive performance and light exposure, at scale, and during everyday life. To this end, we generated an app (Brighter Time) which incorporated a psychomotor vigilance (PVT), an N-back and a visual search task with questionnaire-based assessments of demographic characteristics, general health, chronotype and sleep. The app also measured illuminance during task completion using the smartphone's intrinsic light meter. We undertook a pilot feasibility study of Brighter Time based on 91-week-long acquisition phases within a convenience sample (recruited by local advertisements and word of mouth) running Brighter Time on their own smartphones over two study phases in winter and summer. Study compliance was suitable (median = 20/21 requested task completions per subject). Statistically significant associations were observed between subjective sleepiness and performance in all tasks. Significant daily variations in PVT and visual search performance were also observed. Higher illuminance was associated with reduced reaction time and lower inverse efficiency score in the visual search. Brighter Time thus represents a viable option for large-scale collection of cognitive task data in everyday life, and is able to reveal associations between task performance and sleepiness, time of day and current illuminance. Brighter Time's utility could be extended to exploring associations with longer-term patterns of light exposure and/or other light metrics by integrating with wearable light meters.

Assessing functional reorganization in visual cortex with simulated retinal lesions.

Macular degeneration (MD) causes central vision loss, removing input to corresponding representations in the primary visual cortex. There is disagreement concerning whether the cortical regions deprived of input can remain responsive, and the source of reported cortical responses is still debated. To simulate MD in controls, normally sighted participants viewed a bright central disk to adapt the retina, creating a transient 'retinal lesion' during a functional MRI experiment. Participants viewed blocks of faces, scrambled faces and uniform grey stimuli, either passively or whilst performing a one-back task. To assess the impact of the simulated lesion, participants repeated the paradigm using a more conventional mean luminance simulated scotoma without adaptation. Our results suggest our attempt to create a more realistic simulation of a lesion did not impact on responses in the representation of the simulated lesion. While most participants showed no evidence of stimulus-driven activation within the lesion representation, a few individuals (22%) exhibited responses similar to a participant with juvenile MD who completed the same paradigm (without adaptation). Reliability analysis showed that responses in the representation of the lesion were generally consistent irrespective of whether positive or negative. We provide some evidence that peripheral visual stimulation can also produce responses in central representations in controls while performing a task. This suggests that the 'signature of reorganization of visual processing', is not found solely in patients with retinal lesions, consistent with the idea that activity may be driven by unmasked top-down feedback.

Laminar Organization of Working Memory Signals in Human Visual Cortex.

The human primary visual cortex (V1) is not only activated by incoming visual information but is also engaged by top-down cognitive processes, such as visual working memory, even in the absence of visual input [1-3]. This feedback may be critical to our ability to visualize specific visual features, as higher-order regions lack the selectivity to represent such information [4]. Clearly, such internally generated signals do not trigger genuine perception of the remembered stimulus, meaning they must be organized in a manner that is different to bottom-up-driven signals. Internally generated signals may be kept separate from incoming sensory data by virtue of the laminar organization of inter-area cortical connections. Namely, bottom-up driving connections target layer 4, located in the middle of the cortical column, and feedback connections target deep and superficial layers and avoid layer 4 [5-7]. Using lamina-resolved fMRI, we simultaneously measured the activity in three early visual cortical areas (V1-V3) that are recruited to represent stimulus information during visual working memory [8]. We observed item-specific working memory signals in early visual cortex. In V1, this item-specific activity was selectively present at deep and superficial cortical depths, avoiding the middle layers, and working-memory-related activity was present at all depths in V2 and V3. These results show for the first time the laminar organization of internally generated signals during visual working memory in the human visual system and provide new insights into how bottom-up and top-down signals in visual cortex are deployed.