Differential cortical and subcortical visual processing with eyes shut.

Closing our eyes largely shuts down our ability to see. That said, our eyelids still pass some light, allowing our visual system to coarsely process information about visual scenes, such as changes in luminance. However, the specific impact of eye closure on processing within the early visual system remains largely unknown. To understand how visual processing is modulated when eyes are shut, we used functional magnetic resonance imaging (fMRI) to measure responses to a flickering visual stimulus at high (100%) and low (10%) temporal contrasts, while participants viewed the stimuli with their eyes open or closed. Interestingly, we discovered that eye closure produced a qualitatively distinct pattern of effects across the visual thalamus and visual cortex. We found that with eyes open, low temporal contrast stimuli produced smaller responses across the lateral geniculate nucleus (LGN), primary (V1) and extrastriate visual cortex (V2). However, with eyes closed, we discovered that the LGN and V1 maintained similar blood oxygenation level-dependent (BOLD) responses as the eyes open condition, despite the suppressed visual input through the eyelid. In contrast, V2 and V3 had strongly attenuated BOLD response when eyes were closed, regardless of temporal contrast. Our findings reveal a qualitatively distinct pattern of visual processing when the eyes are closed-one that is not simply an overall attenuation but rather reflects distinct responses across visual thalamocortical networks, wherein the earliest stages of processing preserve information about stimuli but are then gated off downstream in visual cortex.NEW & NOTEWORTHY When we close our eyes coarse luminance information is still accessible by the visual system. Using functional magnetic resonance imaging, we examined whether eyelid closure plays a unique role in visual processing. We discovered that while the LGN and V1 show equivalent responses when the eyes are open or closed, extrastriate cortex exhibited attenuated responses with eye closure. This suggests that when the eyes are closed, downstream visual processing is blind to this information.

(Don't) look where you are going: Evidence for a travel direction signal in humans that is independent of head direction.

We often assume that travel direction is redundant with head direction, but from first principles, these two factors provide differing spatial information. Although head direction has been found to be a fundamental component of human navigation, it is unclear how self-motion signals for travel direction contribute to forming a travel trajectory. Employing a novel motion adaptation paradigm from visual neuroscience designed to preclude a contribution of head direction, we found high-level aftereffects of perceived travel direction, indicating that travel direction is a fundamental component of human navigation. Interestingly, we discovered a higher frequency of reporting perceived travel toward the adapted direction compared to a no-adapt control-an aftereffect that runs contrary to low-level motion aftereffects. This travel aftereffect was maintained after controlling for possible response biases and approaching effects, and it scaled with adaptation duration. These findings demonstrate the first evidence of how a pure travel direction signal might be represented in humans, independent of head direction. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Attention preserves the selectivity of feature-tuned normalization.

Attention and divisive normalization both contribute to making visual processing more efficient. Attention selectively increases the neural gain of relevant information in the early visual cortex, resulting in stronger perceived salience for attended regions or features. Divisive normalization improves processing efficiency by suppressing responses to homogeneous inputs and highlighting salient boundaries, facilitating sparse coding of inputs. Theoretical and empirical research suggest a tight link between attention and normalization, wherein attending to a stimulus results in a release from normalization, thereby allowing for an increase in neural response gain. In the present study, we address whether attention alters the qualitative properties of normalization. Specifically, we examine how attention influences the feature-tuned nature of normalization, whereby suppression is stronger between visual stimuli whose orientation contents are similar, and weaker when the orientations are different. Ten human observers viewed stimuli that varied in orientation content while we acquired fMRI BOLD responses under two attentional states: attending toward or attending away from the stimulus. Our results indicate that attention does not alter the specificity of feature-tuned normalization. Instead, attention seems to enhance visuocortical responses evenly, regardless of the degree of orientation similarity within the stimulus. Since visuocortical responses exhibit adaptation to statistical regularities in natural scenes, we conclude that while attention can selectively increase the gain of responses to attended items, it does not appear to alter the ecologically relevant correspondence between orientation differences and strength of tuned normalization.NEW & NOTEWORTHY The magnitude of visuocortical BOLD responses scales with orientation differences in visual stimuli, with the strongest response suppression for collinear stimuli and least suppression for orthogonal, in a way that appears to match natural scene statistics. We examined the effects of attention on this feature-tuned property of suppression and found that while attending to a stimulus increases the overall gain of visuocortical responses, the qualitative properties of feature-tuning remain unchanged, suggesting attention preserves tuned normalization properties.

Differential cortical and subcortical visual processing with eyes shut.

Closing our eyes largely shuts down our ability to see. That said, our eyelids still pass some light, allowing our visual system to coarsely process information about visual scenes, such as changes in luminance. However, the specific impact of eye closure on processing within the early visual system remains largely unknown. To understand how visual processing is modulated when eyes are shut, we used functional magnetic resonance imaging (fMRI) to measure responses to a flickering visual stimulus at high (100%) and low (10%) temporal contrasts, while participants viewed the stimuli with their eyes open or closed. Interestingly, we discovered that eye closure produced a qualitatively distinct pattern of effects across the visual thalamus and visual cortex. We found that with eyes open, low temporal contrast stimuli produced smaller responses, across the lateral geniculate nucleus (LGN), primary (V1) and extrastriate visual cortex (V2). However, with eyes closed, we discovered that the LGN and V1 maintained similar BOLD responses as the eyes open condition, despite the suppressed visual input through the eyelid. In contrast, V2 and V3 had strongly attenuated BOLD response when eyes were closed, regardless of temporal contrast. Our findings reveal a qualitative distinct pattern of visual processing when the eyes are closed - one that is not simply an overall attenuation, but rather reflects distinct responses across visual thalamocortical networks, wherein the earliest stages of processing preserves information about stimuli but is then gated off downstream in visual cortex.

The cost of divided attention for detection of simple visual features primarily reflects limits in post-perceptual processing.

Covert spatial attention allows us to prioritize processing at relevant locations. Perception is generally poorer when attention is distributed across multiple locations than when attention is focused on a single location. However, while divided attention typically impairs performance, recent work suggests that divided attention does not seem to impair detection of simple visual features. Here, we re-examined this possibility. In two experiments, observers detected a simple target (a vertical Gabor), and we manipulated whether attention was focused at one location (focal-cue condition) or distributed across two locations (distributed-cue condition). In Experiment 1, targets could appear independently at each location, such that observers needed to judge target presence for each location separately in the distributed-cue condition. Under these conditions, we found a robust cost of dividing attention. Next, we further probed what stage of processing gave rise to this cost. In Experiment 1, the cost of dividing attention could reflect a limit in the ability to make concurrent judgments about target presence. In Experiment 2, we simplified the task to test whether this was the case: just one target could appear on each trial, such that observers made a single judgment ("was a target present?") in both the focal-cue and distributed-cue conditions. Here, we found a marginal cost of dividing attention that was weaker than the cost in Experiment 1. Together, our results suggest that divided attention does impair detection of simple visual features, but that this cost is primarily due to a limit in post-perceptual processes.

Feature-based attention multiplicatively scales the fMRI-BOLD contrast-response function.

Functional MRI (fMRI) plays a key role in the study of attention. However, there remains a puzzling discrepancy between attention effects measured with fMRI and with electrophysiological methods. While electrophysiological studies find that attention increases sensory gain, amplifying stimulus-evoked neural responses by multiplicatively scaling the contrast-response function (CRF), fMRI appears to be insensitive to these multiplicative effects. Instead, fMRI studies typically find that attention produces an additive baseline shift in the blood-oxygen-level-dependent (BOLD) signal. These findings suggest that attentional effects measured with fMRI reflect top-down inputs to visual cortex, rather than the modulation of sensory gain. If true, this drastically limits what fMRI can tell us about how attention improves sensory coding. Here, we examined whether fMRI is sensitive to multiplicative effects of attention using a feature-based attention paradigm designed to preclude any possible additive effects. We measured BOLD activity evoked by a probe stimulus in one visual hemifield while participants (6 male, 6 female) attended to the probe orientation (attended condition), or to an orthogonal orientation (unattended condition), in the other hemifield. To measure CRFs in visual areas V1-V3, we parametrically varied the contrast of the probe stimulus. In all three areas, feature-based attention increased contrast gain, improving sensitivity by shifting CRFs towards lower contrasts. In V2 and V3, we also found an increase in response gain, an increase in the responsivity of the CRF, that was greatest at inner eccentricities. These results provide clear evidence that the fMRI-BOLD signal is sensitive to multiplicative effects of attention.SIGNIFICANCE STATEMENTFunctional MRI (fMRI) plays a central role in the study of attention because it allows researchers to precisely and non-invasively characterize the effects of attention throughout the brain. Electrophysiological studies have shown that attention increases sensory gain, amplifying stimulus-evoked neural responses. However, a growing body of work suggests that the BOLD signal that is measured with fMRI is not sensitive to these multiplicative effects of attention, calling into question what we can learn from fMRI about how attention improves sensory codes. Here, using a feature-based attention paradigm, we provide evidence that the BOLD signal can pick up multiplicative effects of attention.

Arousal-based pupil modulation is dictated by luminance.

Pupillometry has become a standard measure for assessing arousal state. However, environmental factors such as luminance, a primary dictator of pupillary responses, often vary across studies. To what degree does luminance interact with arousal-driven pupillary changes? Here, we parametrically assessed luminance-driven pupillary responses across a wide-range of luminances, while concurrently manipulating cognitive arousal using auditory math problems of varying difficulty. At the group-level, our results revealed that the modulatory effect of cognitive arousal on pupil size interacts multiplicatively with luminance, with the largest effects occurring at low and mid-luminances. However, at the level of individuals, there were qualitatively distinct individual differences in the modulatory effect of cognitive arousal on luminance-driven pupillary responses. Our findings suggest that pupillometry as a measure for assessing arousal requires more careful consideration: there are ranges of luminance levels that are more ideal in observing pupillary differences between arousal conditions than others.

Saturating Nonlinearities of Contrast Response in Human Visual Cortex.

Response nonlinearities are ubiquitous throughout the brain, especially within sensory cortices where changes in stimulus intensity typically produce compressed responses. Although this relationship is well established in electrophysiological measurements, it remains controversial whether the same nonlinearities hold for population-based measurements obtained with human fMRI. We propose that these purported disparities are not contingent on measurement type and are instead largely dependent on the visual system state at the time of interrogation. We show that deploying a contrast adaptation paradigm permits reliable measurements of saturating sigmoidal contrast response functions (10 participants, 7 female). When not controlling the adaptation state, our results coincide with previous fMRI studies, yielding nonsaturating, largely linear contrast responses. These findings highlight the important role of adaptation in manifesting measurable nonlinear responses within human visual cortex, reconciling discrepancies reported in vision neuroscience, re-establishing the qualitative relationship between stimulus intensity and response across different neural measures and the concerted study of cortical gain control.SIGNIFICANCE STATEMENT Nonlinear stimulus-response relationships govern many essential brain functions, ranging from the sensory to cognitive level. Certain core response properties previously shown to be nonlinear with nonhuman electrophysiology recordings have yet to be reliably measured with human neuroimaging, prompting uncertainty and reconsideration. The results of this study stand to reconcile these incongruencies in the vision neurosciences, demonstrating the profound impact adaptation can have on brain activation throughout the early visual cortex. Moving forward, these findings facilitate the study of modulatory influences on sensory processing (i.e., arousal and attention) and help establish a closer link between neural recordings in animals and hemodynamic measurements from human fMRI, resuming a concerted effort to understand operations in the mammalian cortex.

The specificity of orientation-tuned normalization within human early visual cortex.

Normalization within visual cortex is modulated by contextual influences; stimuli sharing similar features suppress each other more than dissimilar stimuli. This feature-tuned component of suppression depends on multiple factors, including the orientation content of stimuli. Indeed, pairs of stimuli arranged in a center-surround configuration attenuate each other's response to a greater degree when oriented collinearly than when oriented orthogonally. Although numerous studies have examined the nature of surround suppression at these two extremes, far less is known about how the strength of tuned normalization varies as a function of continuous changes in orientation similarity, particularly in humans. In this study, we used functional magnetic resonance imaging (fMRI) to examine the bandwidth of orientation-tuned suppression within human visual cortex. Blood-oxygen-level-dependent (BOLD) responses were acquired as participants viewed a full-field circular stimulus composed of wedges of orientation-bandpass filtered noise. This stimulus configuration allowed us to parametrically vary orientation differences between neighboring wedges in gradual steps between collinear and orthogonal. We found the greatest suppression for collinearly arranged stimuli with a gradual increase in BOLD response as the orientation content became more dissimilar. We quantified the tuning width of orientation-tuned suppression, finding that the voxel-wise bandwidth of orientation tuned normalization was between 20° and 30°, and did not differ substantially between early visual areas. Voxel-wise analyses revealed that suppression width covaried with retinotopic preference, with the tightest bandwidths at outer eccentricities. Having an estimate of orientation-tuned suppression bandwidth can serve to constrain models of tuned normalization, establishing the precise degree to which suppression strength depends on similarity between visual stimulus components.NEW & NOTEWORTHY Neurons in the early visual cortex are subject to divisive normalization, but the feature-tuning aspect of this computation remains understudied, particularly in humans. We investigated orientation tuning of normalization in human early visual cortex using fMRI and estimated the bandwidth of the tuned normalization function across observers. Our findings provide a characterization of tuned normalization in early visual cortex that could help constrain models of divisive normalization in vision.

Temporal attention selectively enhances target features.

Temporal attention, the allocation of attention to a moment in time, improves perception. Here, we examined the computational mechanism by which temporal attention improves perception, under a divisive normalization framework. Under this framework, attention can improve perception of a target signal in three ways: stimulus enhancement (increasing gain across all sensory channels), signal enhancement (selectively increasing gain in channels that encode the target stimulus), or external noise exclusion (reducing the gain in channels that encode irrelevant features). These mechanisms make diverging predictions when a target is embedded in varying levels of noise: stimulus enhancement improves performance only when noise is low, signal enhancement improves performance at all noise intensities, and external noise exclusion improves performance only when noise is high. To date, temporal attention studies have used noise-free displays. Therefore, it is unclear whether temporal attention acts via stimulus enhancement (amplifying both target features and noise) or signal enhancement (selectively amplifying target features) because both mechanisms predict improved performance in the absence of noise. To tease these mechanisms apart, we manipulated temporal attention using an auditory cue while parametrically varying external noise in a fine-orientation discrimination task. Temporal attention improved perceptual thresholds across all noise levels. Formal model comparisons revealed that this cuing effect was best accounted for by a combination of signal enhancement and stimulus enhancement, suggesting that temporal attention improves perceptual performance, in part, by selectively increasing gain for target features.

Dual strategies in human confidence judgments.

Although confidence is commonly believed to be an essential element in decision-making, it remains unclear what gives rise to one's sense of confidence. Recent Bayesian theories propose that confidence is computed, in part, from the degree of uncertainty in sensory evidence. Alternatively, observers can use physical properties of the stimulus as a heuristic to confidence. In the current study, we developed ideal observer models for either hypothesis and compared their predictions against human data obtained from psychophysical experiments. Participants reported the orientation of a stimulus, and their confidence in this estimate, under varying levels of internal and external noise. As predicted by the Bayesian model, we found a consistent link between confidence and behavioral variability for a given stimulus orientation. Confidence was higher when orientation estimates were more precise, for both internal and external sources of noise. However, we observed the inverse pattern when comparing between stimulus orientations: although observers gave more precise orientation estimates for cardinal orientations (a phenomenon known as the oblique effect), they were more confident about oblique orientations. We show that these results are well explained by a strategy to confidence that is based on the perceived amount of noise in the stimulus. Altogether, our results suggest that confidence is not always computed from the degree of uncertainty in one's perceptual evidence but can instead be based on visual cues that function as simple Heuristics to confidence.

Conflict defined by global gestalt can modulate binocular rivalry suppression.

Binocular rivalry suppression is thought to necessarily require local interocular conflict: the presence of incompatible image elements, such as orthogonal contours, in retinally corresponding regions of two monocular displays. Whether suppression can also be driven by conflict at the level of spatially nonlocal surface or object representations is unclear. Here, we kept local contour conflict constant while varying global conflict, defined by the gestalt formed by the two monocular displays. Specifically, each eye was presented with a grid of image elements (crosses or plusses), placed such that the two eyes' individual grid elements did not directly overlap but the grids as a whole did. In a "shared motion" condition, all elements moved in unison, inviting a gestalt made up of all elements across both eyes; in a "different motions" condition, the elements' trajectories differed between eyes, inviting a gestalt of two overlapping surfaces, each associated with one eye. Perceptual disappearances of image elements occurred more readily in the different motions condition, an observation that could not be explained by any between-condition differences in local contour conflict. In a second experiment, we furthermore established that, whereas perceptual disappearances in the shared motion condition tended to involve a single element at a time, in the different motions condition, multiple elements belonging to the same gestalt often disappeared together. These findings indicate that, even though binocular rivalry may critically rely on inhibition due to locally incompatible image elements, this inhibition also depends on the global gestalt to which these elements contribute.

Population spatial frequency tuning in human early visual cortex.

Neurons within early visual cortex are selective for basic image statistics, including spatial frequency. However, these neurons are thought to act as band-pass filters, with the window of spatial frequency sensitivity varying across the visual field and across visual areas. Although a handful of previous functional (f)MRI studies have examined human spatial frequency sensitivity using conventional designs and analysis methods, these measurements are time consuming and fail to capture the precision of spatial frequency tuning (bandwidth). In this study, we introduce a model-driven approach to fMRI analyses that allows for fast and efficient estimation of population spatial frequency tuning (pSFT) for individual voxels. Blood oxygen level-dependent (BOLD) responses within early visual cortex were acquired while subjects viewed a series of full-field stimuli that swept through a large range of spatial frequency content. Each stimulus was generated by band-pass filtering white noise with a central frequency that changed periodically between a minimum of 0.5 cycles/degree (cpd) and a maximum of 12 cpd. To estimate the underlying frequency tuning of each voxel, we assumed a log-Gaussian pSFT and optimized the parameters of this function by comparing our model output against the measured BOLD time series. Consistent with previous studies, our results show that an increase in eccentricity within each visual area is accompanied by a drop in the peak spatial frequency of the pSFT. Moreover, we found that pSFT bandwidth depends on eccentricity and is correlated with the pSFT peak; populations with lower peaks possess broader bandwidths in logarithmic scale, whereas in linear scale this relationship is reversed.NEW & NOTEWORTHY Spatial frequency selectivity is a hallmark property of early visuocortical neurons, and mapping these sensitivities gives us crucial insight into the hierarchical organization of information within visual areas. Due to technical obstacles, we lack a comprehensive picture of the properties of this sensitivity in humans. Here, we introduce a new method, coined population spatial frequency tuning mapping, which circumvents the limitations of the conventional neuroimaging methods, yielding a fuller visuocortical map of spatial frequency sensitivity.

Luminance potentiates human visuocortical responses.

Our visual system is tasked with transforming variations in light within our environment into a coherent percept, typically described using properties such as luminance and contrast. Models of vision often downplay the importance of luminance in shaping cortical responses, instead prioritizing representations that do not covary with overall luminance (i.e., contrast), and yet visuocortical response properties that may reflect luminance encoding remain poorly understood. In this study, we examined whether well-established visuocortical response properties may also reflect luminance encoding, challenging the idea that luminance information itself plays no significant role in supporting visual perception. To do so, we measured functional activity in human visual cortex when presenting stimuli varying in contrast and mean luminance, and found that luminance response functions are strongly contrast dependent between 50 and 250 cd/m2, confirmed with a subsequent experiment. High-contrast stimuli produced linearly increasing responses as luminance increased logarithmically for all early visual areas, whereas low-contrast stimuli produced either flat (V1) or assorted positive linear (V2 and V3) response profiles. These results reveal that the mean luminance information of a visual signal persists within visuocortical representations, potentially reflecting an inherent imbalance of excitatory and inhibitory components that can be either contrast dependent (V1 and V2) or contrast invariant (V3). The role of luminance should be considered when the aim is to drive potent visually evoked responses and when activity is compared across studies. More broadly, overall luminance should be weighed heavily as a core feature of the visual system and should play a significant role in cortical models of vision.NEW & NOTEWORTHY This neuroimaging study investigates the influence of overall luminance on population activity in human visual cortex. We discovered that the response to a particular stimulus contrast level is reliant, in part, on the mean luminance of a signal, revealing that the mean luminance information of our environment is represented within the visual cortex. The results challenge a long-standing misconception about the role of luminance information in the processing of visual information at the cortical level.

Normalization governs attentional modulation within human visual cortex.

Although attention is known to increase the gain of visuocortical responses, its underlying neural computations remain unclear. Here, we use fMRI to test the hypothesis that a neural population's ability to be modulated by attention is dependent on divisive normalization. To do so, we leverage the feature-tuned properties of normalization and find that visuocortical responses to stimuli sharing features normalize each other more strongly. Comparing these normalization measures to measures of attentional modulation, we demonstrate that subpopulations which exhibit stronger normalization also exhibit larger attentional benefits. In a converging experiment, we reveal that attentional benefits are greatest when a subpopulation is forced into a state of stronger normalization. Taken together, these results suggest that the degree to which a subpopulation exhibits normalization plays a role in dictating its potential for attentional benefits.

Dichoptic vision in the absence of attention: neither fusion nor rivalry.

When the two eyes' processing streams meet in visual cortex, two things can happen: sufficiently similar monocular inputs are combined into a fused representation, whereas markedly different inputs engage in rivalry. Interestingly, the emergence of rivalry appears to require attention. Withdrawing attention causes the alternating monocular dominance that characterizes rivalry to cease, apparently allowing both monocular signals to be processed simultaneously. What happens to these signals in this case, however, remains something of a mystery; are they fused into an integrated representation? In a set of experiments, we show this not to be the case: visual aftereffects are consistent with the simultaneous yet separate presence of two segregated monocular representations, rather than a joint representation. These results provide evidence that dichoptic vision without attention prompts a third and previously unknown mode, where both eyes' inputs receive equal processing, but escape interocular fusion.

Visuocortical changes during a freezing-like state in humans.

An adaptive response to threat requires optimized detection of critical sensory cues. This optimization is thought to be aided by freezing - an evolutionarily preserved defensive state of immobility characterized by parasympathetically mediated fear bradycardia and regulated by the amygdala-periaqueductal grey (PAG) circuit. Behavioral observations in humans and animals have suggested that freezing is also a state of enhanced visual sensitivity, particularly for coarse visual information, but the underlying neural mechanisms remain unclear. We induced a freezing-like state in healthy volunteers using threat of electrical shock and measured threat-related changes in both stimulus-independent (baseline) and stimulus-evoked visuocortical activity to low-vs. high-spatial frequency gratings, using functional MRI. As measuring immobility is not feasible in MRI environments, we used fear bradycardia and amygdala-PAG coupling in inferring a freezing-like state. An independent functional localizer and retinotopic mapping were used to assess the retinotopic specificity of visuocortical modulations. We found a threat-induced increase in baseline (stimulus-independent) visuocortical activity that was retinotopically nonspecific, which was accompanied by increased connectivity with the amygdala. A positive correlation between visuocortical activity and fear bradycardia (while controlling for sympathetic activation), and a concomitant increase in amygdala-PAG connectivity, confirmed the specificity of these findings for the parasympathetically dominated freezing-like state. Visuocortical responses to gratings were retinotopically specific, but did not differ between threat and safe conditions across participants. However, individuals who exhibited better discrimination of low-spatial frequency stimuli showed reduced stimulus-evoked V1 responses under threat. Our findings suggest that a defensive state of freezing involves an integration of preparatory defensive and perceptual changes which may be regulated by a common mechanism involving the amygdala.

Visual Memories Bypass Normalization.

How distinct are visual memory representations from visual perception? Although evidence suggests that briefly remembered stimuli are represented within early visual cortices, the degree to which these memory traces resemble true visual representations remains something of a mystery. Here, we tested whether both visual memory and perception succumb to a seemingly ubiquitous neural computation: normalization. Observers were asked to remember the contrast of visual stimuli, which were pitted against each other to promote normalization either in perception or in visual memory. Our results revealed robust normalization between visual representations in perception, yet no signature of normalization occurring between working memory stores-neither between representations in memory nor between memory representations and visual inputs. These results provide unique insight into the nature of visual memory representations, illustrating that visual memory representations follow a different set of computational rules, bypassing normalization, a canonical visual computation.