Responses In Early Visual Cortex Research Articles

Task-related hemodynamic responses in human early visual cortex are modulated by task difficulty and behavioral performance.

Early visual cortex exhibits widespread hemodynamic responses in the absence of visual stimulation, which are entrained to the timing of a task and not predicted by local spiking or local field potential. Such task-related responses (TRRs) covary with reward magnitude and physiological signatures of arousal. It is unknown, however, if TRRs change on a trial-to-trial basis according to behavioral performance and task difficulty. If so, this would suggest that TRRs reflect arousal on a trial-to-trial timescale and covary with critical task and behavioral variables. We measured functional magnetic resonance imaging blood-oxygen-level-dependent (fMRI-BOLD) responses in the early visual cortex of human observers performing an orientation discrimination task consisting of separate easy and hard runs of trials. Stimuli were presented in a small portion of one hemifield, but the fMRI response was measured in the ipsilateral hemisphere, far from the stimulus representation and focus of spatial attention. TRRs scaled in amplitude with task difficulty, behavioral accuracy, reaction time, and lapses across trials. These modulations were not explained by the influence of respiration, cardiac activity, or head movement on the fMRI signal. Similar modulations with task difficulty and behavior were observed in pupil size. These results suggest that TRRs reflect arousal and behavior on the timescale of individual trials.

Apparent Motion Induces Activity Suppression in Early Visual Cortex and Impairs Visual Detection.

Apparent motion (AM) is induced when two stationary visual stimuli are presented in alternating sequence. Intriguingly, AM leads to an impaired detectability of stimuli along the AM path (i.e., AM-induced masking). It has been hypothesized that AM triggers an internal representation of a moving object in early visual cortex, which competes with stimulus-evoked representations of visual stimuli on the motion path in early visual cortex of 25 human adults (16 female). We tested this hypothesis by measuring BOLD responses in early visual cortex during the process of AM-induced masking, using fMRI and population receptive field methods. Surprisingly, and counter to our hypothesis, we showed that AM suppressed, rather than increased, BOLD responses along early visual (V1 and V2) representations of the AM path, including regions that were not directly activated by the AM inducer stimuli. This activity suppression of the visual response predicted the subsequent reduction in detectability of the target that appeared in the middle of the AM path. Our data thereby provide direct empirical evidence for suppressive neural mechanisms underlying AM and suggest that illusory motion can render us blind to objects on the motion path by suppressing neural activity at the earliest cortical stages of visual perception.SIGNIFICANCE STATEMENT When two spatially distinct visual objects are presented in alternating sequence, apparent motion (AM) occurs and impairs detectability of stimuli along its path. The underlying mechanism is thought to be that increased activation in human early visual cortex evoked by AM interferes with the representation of the stimulus. Strikingly, however, we show that AM suppresses neural activity along the motion path, and the strength of activity suppression predicts the subsequent behavioral performance decrement in terms of detecting a stimulus along the AM path. Our findings provide empirical evidence for a suppressive, rather than faciliatory, mechanism underlying AM.

Value-driven attentional capture enhances distractor representations in early visual cortex.

When a behaviorally relevant stimulus has been previously associated with reward, behavioral responses are faster and more accurate compared to equally relevant but less valuable stimuli. Conversely, task-irrelevant stimuli that were previously associated with a high reward can capture attention and distract processing away from relevant stimuli (e.g., seeing a chocolate bar in the pantry when you are looking for a nice, healthy apple). Although increasing the value of task-relevant stimuli systematically up-regulates neural responses in early visual cortex to facilitate information processing, it is not clear whether the value of task-irrelevant distractors influences behavior via competition in early visual cortex or via competition at later stages of decision-making and response selection. Here, we measured functional magnetic resonance imaging (fMRI) in human visual cortex while subjects performed a value-based learning task, and we applied a multivariate inverted encoding model (IEM) to assess the fidelity of distractor representations in early visual cortex. We found that the fidelity of neural representations related to task-irrelevant distractors increased when the distractors were previously associated with a high reward. This finding suggests that value-driven attentional capture begins with sensory modulations of distractor representations in early areas of visual cortex.

Coexisting representations of sensory and mnemonic information in human visual cortex.

Traversing sensory environments requires keeping relevant information in mind while simultaneously processing new inputs. Visual information is kept in working memory via feature selective responses in early visual cortex, but recent work had suggested that new sensory inputs obligatorily wipe out this information. Here we show region-wide multiplexing abilities in classic sensory areas, with population-level response patterns in early visual cortex representing the contents of working memory alongside new sensory inputs. In a second experiment, we show that when people get distracted, this leads to both disruptions of mnemonic information in early visual cortex and decrements in behavioral recall. Representations in the intraparietal sulcus reflect actively remembered information encoded in a transformed format, but not task-irrelevant sensory inputs. Together these results suggest that early visual areas play a key role in supporting high resolution working memory representations that can serve as a template for comparing incoming sensory information.

The time course of different surround suppression mechanisms.

What we see depends on the spatial context in which it appears. Previous work has linked the suppression of perceived contrast by surrounding stimuli to reduced neural responses in early visual cortex. This surround suppression depends on at least two separable neural mechanisms, “low-level” and “higher level,” which can be differentiated by their response characteristics. We used electroencephalography to demonstrate for the first time that human occipital neural responses show evidence of these two suppression mechanisms. Eighteen adults (10 women, 8 men) each participated in three experimental sessions, in which they viewed visual stimuli through a mirror stereoscope. The first session was used to identify the C1 component, while the second and third comprised the main experiment. Event-related potentials were measured in response to center gratings either with no surround or with surrounding gratings oriented parallel or orthogonal, and presented in either the same eye (monoptic) or the opposite eye (dichoptic). We found that the earliest component of an event-related potential (C1; ∼60 ms) was suppressed by surrounding stimuli, but that suppression did not depend on surround configuration. This suggests a suppression mechanism that is not tuned for relative orientation acting on the earliest cortical response to the target. A later response component (N1; ∼160 ms) showed stronger suppression for parallel and monoptic surrounds, consistent with our earlier psychophysical results and a second form of suppression that is binocular and orientation tuned. We conclude that these two forms of surround suppression have distinct response time courses in the human visual system, which can be differentiated using electrophysiology.

Scene complexity modulates degree of feedback activity during object detection in natural scenes.

Selective brain responses to objects arise within a few hundreds of milliseconds of neural processing, suggesting that visual object recognition is mediated by rapid feed-forward activations. Yet disruption of neural responses in early visual cortex beyond feed-forward processing stages affects object recognition performance. Here, we unite these discrepant findings by reporting that object recognition involves enhanced feedback activity (recurrent processing within early visual cortex) when target objects are embedded in natural scenes that are characterized by high complexity. Human participants performed an animal target detection task on natural scenes with low, medium or high complexity as determined by a computational model of low-level contrast statistics. Three converging lines of evidence indicate that feedback was selectively enhanced for high complexity scenes. First, functional magnetic resonance imaging (fMRI) activity in early visual cortex (V1) was enhanced for target objects in scenes with high, but not low or medium complexity. Second, event-related potentials (ERPs) evoked by target objects were selectively enhanced at feedback stages of visual processing (from ~220 ms onwards) for high complexity scenes only. Third, behavioral performance for high complexity scenes deteriorated when participants were pressed for time and thus less able to incorporate the feedback activity. Modeling of the reaction time distributions using drift diffusion revealed that object information accumulated more slowly for high complexity scenes, with evidence accumulation being coupled to trial-to-trial variation in the EEG feedback response. Together, these results suggest that while feed-forward activity may suffice to recognize isolated objects, the brain employs recurrent processing more adaptively in naturalistic settings, using minimal feedback for simple scenes and increasing feedback for complex scenes.

Hyper-upregulation of abnormally low neural response along the visual pathway in autism

A unifying theme of numerous proposals of the pathophysiology of autism spectrum disorder (ASD) is that it results from a pervasive alteration in neural excitability. However, the various forms of evidence implicating neural excitability appear contradictory. On one hand, a well-known hypothesis is that ASD might reflect an increase in excitation/inhibition (E/I) balance and hyper-excitability of cortical circuits. However, other evidence from animal models has pointed to the opposite hypothesis – that ASD can be characterized by a reduction in E/I balance resulting from reduced excitability. It has recently been suggested that both perspectives – over- and under-excitability – can be reconciled in a framework that takes into account the propagation of information in neural circuits and homeostatic mechanisms that stabilize neural responses. We used the well-established hierarchical structure of human visual motion processing to test the hypothesis that there is abnormal coupling of responses between visual areas in individuals with ASD. We used fMRI to measure neural responses to moving gratings of varying contrast in early visual cortex (EVC) and in human MT complex (hMT+), a motion selective region in the lateral occipital lobe that receives direct input from EVC. Our findings demonstrate that, among neurotypical participants, neural response magnitudes correlate between these brain regions: individuals with relatively high responses in EVC also have high responses in hMT+. On the contrary, among individuals with autism, there is a negative relationship between the magnitude of contrast responses in EVC and the magnitude of response in hMT+. Specifically, participants with abnormally low responses in EVC exhibit abnormally high responses in hMT+. Interestingly, the degree of abnormality in the neural responses correlates with severity of clinical symptoms of ASD. Our findings may suggest that compensatory homeostatic processes are dysregulated along the visual pathway, over-enhancing signals as they propagate through the visual system. Meeting abstract presented at VSS 2018

Linking V1 Activity to Behavior.

A long-term goal of visual neuroscience is to develop and test quantitative models that account for the moment-by-moment relationship between neural responses in early visual cortex and human performance in natural visual tasks. This review focuses on efforts to address this goal by measuring and perturbing the activity of primary visual cortex (V1) neurons while nonhuman primates perform demanding, well-controlled visual tasks. We start by describing a conceptual approach-the decoder linking model (DLM) framework-in which candidate decoding models take neural responses as input and generate predicted behavior as output. The ultimate goal in this framework is to find the actual decoder-the model that best predicts behavior from neural responses. We discuss key relevant properties of primate V1 and review current literature from the DLM perspective. We conclude by discussing major technological and theoretical advances that are likely to accelerate our understanding of the link between V1 activity and behavior.

Spatially selective responses to Kanizsa and occlusion stimuli in human visual cortex

Early visual cortex responds to illusory contours in which abutting lines or collinear edges imply the presence of an occluding surface, as well as to occluded parts of an object. Here we used functional magnetic resonance imaging (fMRI) and population receptive field (pRF) analysis to map retinotopic responses in early visual cortex using bar stimuli defined by illusory contours, occluded parts of a bar, or subtle luminance contrast. All conditions produced retinotopic responses in early visual field maps even though signal-to-noise ratios were very low. We found that signal-to-noise ratios and coherence with independent high-contrast mapping data increased from V1 to V2 to V3. Moreover, we found no differences of signal-to-noise ratios or pRF sizes between the low-contrast luminance and illusion conditions. We propose that all three conditions mapped spatial attention to the bar location rather than activations specifically related to illusory contours or occlusion.

Decoding the orientation of contrast edges from MEG evoked and induced responses

Visual gamma oscillations have been proposed to subserve perceptual binding, but their strong modulation by diverse stimulus features confounds interpretations of their precise functional role. Overcoming this challenge necessitates a comprehensive account of the relationship between gamma responses and stimulus features. Here we used multivariate pattern analyses on human MEG data to characterize the relationships between gamma responses and one basic stimulus feature, the orientation of contrast edges. Our findings confirmed we could decode orientation information from induced responses in two dominant frequency bands at 24–32 Hz and 50–58 Hz. Decoding was higher for cardinal than oblique orientations, with similar results also obtained for evoked MEG responses. In contrast to multivariate analyses, orientation information was mostly absent in univariate signals: evoked and induced responses in early visual cortex were similar in all orientations, with only exception an inverse oblique effect observed in induced responses, such that cardinal orientations produced weaker oscillatory signals than oblique orientations. Taken together, our results showed multivariate methods are well suited for the analysis of gamma oscillations, with multivariate patterns robustly encoding orientation information and predominantly discriminating cardinal from oblique stimuli.

Lightness computation by the human visual system

A model of achromatic color computation by the human visual system is presented, which is shown to account in an exact quantitative way for a large body of appearance matching data collected with simple visual displays. The model equations are closely related to those of the original Retinex model of Land and McCann. However, the present model differs in important ways from Land and McCann’s theory in that it invokes additional biological and perceptual mechanisms, including contrast gain control, different inherent neural gains for incremental, and decremental luminance steps, and two types of top-down influence on the perceptual weights applied to local luminance steps in the display: edge classification and spatial integration attentional windowing. Arguments are presented to support the claim that these various visual processes must be instantiated by a particular underlying neural architecture. By pointing to correspondences between the architecture of the model and findings from visual neurophysiology, this paper suggests that edge classification involves a top-down gating of neural edge responses in early visual cortex (cortical areas V1 and/or V2) while spatial integration windowing occurs in cortical area V4 or beyond.

The tuning of human visual cortex to variations in the 1/fα amplitude spectra and fractal properties of synthetic noise images

Natural scenes share a consistent distribution of energy across spatial frequencies (SF) known as the 1/fα amplitude spectrum (α≈0.8–1.5, mean 1.2). This distribution is scale-invariant, which is a fractal characteristic of natural scenes with statistically similar structure at different spatial scales. While the sensitivity of the visual system to the 1/f properties of natural scenes has been studied extensively using psychophysics, relatively little is known about the tuning of cortical responses to these properties. Here, we use fMRI and retinotopic mapping techniques to measure and analyze BOLD responses in early visual cortex (V1, V2, and V3) to synthetic noise images that vary in their 1/fα amplitude spectra (α=0.25 to 2.25, step size: 0.50) and contrast levels (10% and 30%) (Experiment 1). To compare the dependence of the BOLD response between the photometric (intensity based) and geometric (fractal) properties of our stimuli, in Experiment 2 we compared grayscale noise images to their binary (thresholded) counterparts, which contain only black and white regions. In both experiments, early visual cortex responded maximally to stimuli generated to have an input 1/f slope corresponding to natural 1/fα amplitude spectra, and lower BOLD responses were found for steeper or shallower 1/f slopes (peak modulation: 0.59% for 1.25 vs. 0.31% for 2.25). To control for changing receptive field sizes, responses were also analyzed across multiple eccentricity bands in cortical surface space. For most eccentricity bands, BOLD responses were maximal for natural 1/fα amplitude spectra, but importantly there was no difference in the BOLD response to grayscale stimuli and their corresponding thresholded counterparts. Since the thresholding of an image changes its measured 1/f slope (α) but not its fractal characteristics, this suggests that neuronal responses in early visual cortex are not strictly driven by spectral slope values (photometric properties) but rather their embedded geometric, fractal-like scaling properties.

Continuous Flash Suppression Modulates Cortical Activity in Early Visual Cortex

A salient visual stimulus can be rendered invisible by presenting it to one eye while flashing a mask to the other eye. This procedure, called continuous flash suppression (CFS), has been proposed as an ideal way of studying awareness as it can make a stimulus imperceptible for extended periods of time. Previous studies have reported robust suppression of cortical activity in higher visual areas during CFS, but the role of primary visual cortex (V1) is still controversial. In this study, we resolve this controversy on the role of V1 in CFS and also begin characterizing the computational processes underlying CFS. Early visual cortical activity was measured with functional magnetic resonance imaging while human subjects viewed stimuli composed of target and mask, presented to the same or different eyes. Functional MRI responses in early visual cortex were smaller when target and mask were in different eyes compared with the same eye, not only for the lowest contrast target rendered invisible by CFS, but also for higher contrast targets, which were visible even when presented to the eye opposite the mask. We infer that CFS is based on modulating the gain of neural responses, akin to reducing target contrast.

Contextual effects in human visual cortex depend on surface structure

Neural responses in early visual cortex depend on stimulus context. One of the most well-established context-dependent effects is orientation-specific surround suppression: the neural response to a stimulus inside the receptive field of a neuron ("target") is suppressed when it is surrounded by iso-oriented compared with orthogonal stimuli ("flankers"). Despite the importance of orientation-specific surround suppression in potentially mediating a number of important perceptual effects, including saliency, contour integration, and orientation discrimination, the underlying neural mechanisms remain unknown. The suppressive signal could be inherited from precortical areas as early as the retina and thalamus, arise from local circuits through horizontal connections, or be fed back from higher visual cortex. Here, we show, using two different methodologies, measurements of scalp-recorded event-related potentials (ERPs) and behavioral contrast adaptation aftereffects in humans, that orientation-specific surround suppression is dependent on the surface structure in an image. When the target and flankers can be grouped on the same surface (independent of their distance), orientation-specific surround suppression occurs. When the target and flankers are on different surfaces (independent of their distance), orientation-specific surround suppression does not occur. Our results demonstrate a surprising role of high-level, global processes such as grouping in determining when contextual effects occur in early visual cortex.

The effect of feedback on performance and brain activation during perceptual learning

We investigated the role of informative feedback on the neural correlates of perceptual learning in a coherent-motion detection paradigm. Stimulus displays consisted of four patches of moving dots briefly (500 ms) presented simultaneously, one patch in each visual quadrant. The coherence level was varied in the target patch from near threshold to high, while the other three patches contained only noise. The participants judged whether coherent motion was present or absent in the target patch. To guarantee central fixation, a secondary RSVP digit-detection task was performed at fixation. Over six training sessions subjects learned to detect coherent motion in a predefined quadrant (i.e., the learned location). Half of our subjects were randomly assigned to the feedback group, where they received informative feedback after each response during training, whereas the other group received non-informative feedback during training that a response button was pressed. We investigated whether the presence of informative feedback during training had an influence on the learning success and on the resulting BOLD response. Behavioral data of 24 subjects showed improved performance with increasing practice. Informative feedback promoted learning for motion displays with high coherence levels, whereas it had little effect on learning for displays with near-threshold coherence levels. Learning enhanced fMRI responses in early visual cortex and motion-sensitive area MT+ and these changes were most pronounced for high coherence levels. Activation in the insular and cingulate cortex was mainly influenced by coherence level and trained location. We conclude that feedback modulates behavioral performance and, to a lesser extent, brain activation in areas responsible for monitoring perceptual learning.

Contextual effects in human visual cortex depend on surface structure

Neural responses in early visual cortex depend on stimulus context. One of the most well-established context-dependent effects is orientation-specific surround suppression: the neural response to a...

Decoding Working Memory of Stimulus Contrast in Early Visual Cortex

Most studies of the early stages of visual analysis (V1-V3) have focused on the properties of neurons that support processing of elemental features of a visual stimulus or scene, such as local contrast, orientation, or direction of motion. Recent evidence from electrophysiology and neuroimaging studies, however, suggests that early visual cortex may also play a role in retaining stimulus representations in memory for short periods. For example, fMRI responses obtained during the delay period between two presentations of an oriented visual stimulus can be used to decode the remembered stimulus orientation with multivariate pattern analysis. Here, we investigated whether orientation is a special case or if this phenomenon generalizes to working memory traces of other visual features. We found that multivariate classification of fMRI signals from human visual cortex could be used to decode the contrast of a perceived stimulus even when the mean response changes were accounted for, suggesting some consistent spatial signal for contrast in these areas. Strikingly, we found that fMRI responses also supported decoding of contrast when the stimulus had to be remembered. Furthermore, classification generalized from perceived to remembered stimuli and vice versa, implying that the corresponding pattern of responses in early visual cortex were highly consistent. In additional analyses, we show that stimulus decoding here is driven by biases depending on stimulus eccentricity. This places important constraints on the interpretation for decoding stimulus properties for which cortical processing is known to vary with eccentricity, such as contrast, color, spatial frequency, and temporal frequency.

Continuous flash suppression modulates cortical activity in early visual cortex.

A salient visual stimulus can be rendered invisible by presenting it to one eye while flashing a mask to the other eye. This procedure, called continuous flash suppression (CFS), has been proposed as an ideal way of studying awareness as it can make a stimulus imperceptible for extended periods of time. Previous studies have reported robust suppression of cortical activity in higher visual areas during CFS, but the role of primary visual cortex (V1) is still controversial. In this study, we resolve this controversy on the role of V1 in CFS and also begin characterizing the computational processes underlying CFS. Early visual cortical activity was measured with functional magnetic resonance imaging while human subjects viewed stimuli composed of target and mask, presented to the same or different eyes. Functional MRI responses in early visual cortex were smaller when target and mask were in different eyes compared with the same eye, not only for the lowest contrast target rendered invisible by CFS, but also for higher contrast targets, which were visible even when presented to the eye opposite the mask. We infer that CFS is based on modulating the gain of neural responses, akin to reducing target contrast.

A Two-Stage Cascade Model of BOLD Responses in Human Visual Cortex

Visual neuroscientists have discovered fundamental properties of neural representation through careful analysis of responses to controlled stimuli. Typically, different properties are studied and modeled separately. To integrate our knowledge, it is necessary to build general models that begin with an input image and predict responses to a wide range of stimuli. In this study, we develop a model that accepts an arbitrary band-pass grayscale image as input and predicts blood oxygenation level dependent (BOLD) responses in early visual cortex as output. The model has a cascade architecture, consisting of two stages of linear and nonlinear operations. The first stage involves well-established computations—local oriented filters and divisive normalization—whereas the second stage involves novel computations—compressive spatial summation (a form of normalization) and a variance-like nonlinearity that generates selectivity for second-order contrast. The parameters of the model, which are estimated from BOLD data, vary systematically across visual field maps: compared to primary visual cortex, extrastriate maps generally have larger receptive field size, stronger levels of normalization, and increased selectivity for second-order contrast. Our results provide insight into how stimuli are encoded and transformed in successive stages of visual processing.

Long-Range, Pattern-Dependent Contextual Effects in Early Human Visual Cortex

The standard view of neurons in early visual cortex is that they behave like localized feature detectors. Here we demonstrate that processing in early visual areas goes beyond feature detection by showing that neural responses are greater when a feature deviates from its context compared to when it does not deviate from its context. Using psychophysics, fMRI, and electroencephalography methodologies, we measured neural responses to an oriented Gabor ("target") embedded in various visual patterns as defined by the relative orientation of flanking stimuli. We first show using psychophysical contrast adaptation and fMRI that a target that differs from its context results in more neural activity compared to a target that is contained within an alternating sequence, suggesting that neurons in early visual cortex are sensitive to large-scale orientation patterns. Next, we use event-related potentials to show that orientation deviations affect the earliest sensory components of the target response. Finally, we use forced-choice classification of "noise" stimuli to show that we are more likely to "see" orientations that deviate from the context. Our results suggest that early visual cortex is sensitive to global patterns in images in a way that is markedly different from the predictions of standard models of cortical visual processing.