Signals In Early Visual Cortex Research Articles

Working memory signals in early visual cortex are present in weak and strong imagers.

It has been suggested that visual images are memorized across brief periods of time by vividly imagining them as if they were still there. In line with this, the contents of both working memory and visual imagery are known to be encoded already in early visual cortex. If these signals in early visual areas were indeed to reflect a combined imagery and memory code, one would predict them to be weaker for individuals with reduced visual imagery vividness. Here, we systematically investigated this question in two groups of participants. Strong and weak imagers were asked to remember images across brief delay periods. We were able to reliably reconstruct the memorized stimuli from early visual cortex during the delay. Importantly, in contrast to the prediction, the quality of reconstruction was equally accurate for both strong and weak imagers. The decodable information also closely reflected behavioral precision in both groups, suggesting it could contribute to behavioral performance, even in the extreme case of completely aphantasic individuals. Our data thus suggest that working memory signals in early visual cortex can be present even in the (near) absence of phenomenal imagery.

Poster Session II: Attentional modulation of the achromatic and chromatic reversal VEP.

Previous literature has consistently revealed attentional modulation of the Visual Evoked Potential (VEP) response to achromatic pattern reversal stimuli but little to no attentional modulation of the VEP response to chromatic pattern onsets. Magnetic Resonance Imaging (MRI) research, however, has reported modulation of the responses to both achromatic and chromatic pattern reversal stimuli. Numerous methodological differences including mode of presentation, stimulus contrast, and attentional demand, make comparison of these results difficult. In this study, we report the results of experiments using comparable perceptual contrasts, pattern reversals, and a coextensive and highly-demanding, multiple object tracking (MOT) task. Our findings support prior VEP results indicating that although achromatic VEPs are modulated by attention, chromatic VEPs are more robust to attentional modulation, even for highly demanding distractor tasks. We also found that when compared to a non-attentional condition, the attenuation of the VEP when attending to the MOT task was greater in magnitude than the enhancement of the VEP when attending to the VEP stimulus. This supports prior conclusions, that while avoiding active distraction is likely important, insuring an "attentive state" is not always necessary when recording VEPs. Further experiments are underway to investigate why attentional modulation of chromatic signals in early visual cortex are observed in MRI but not VEP recordings.

Statistical Learning of Frequent Distractor Locations in Visual Search Involves Regional Signal Suppression in Early Visual Cortex.

Observers can learn locations where salient distractors appear frequently to reduce potential interference-an effect attributed to better suppression of distractors at frequent locations. But how distractor suppression is implemented in the visual cortex and within the frontoparietal attention networks remains unclear. We used fMRI and a regional distractor-location learning paradigm with two types of distractors defined in either the same (orientation) or a different (color) dimension to the target to investigate this issue. fMRI results showed that BOLD signals in early visual cortex were significantly reduced for distractors (as well as targets) occurring at the frequent versus rare locations, mirroring behavioral patterns. This reduction was more robust with same-dimension distractors. Crucially, behavioral interference was correlated with distractor-evoked visual activity only for same- (but not different-) dimension distractors. Moreover, with different- (but not same-) dimension distractors, a color-processing area within the fusiform gyrus was activated more when a distractor was present in the rare region versus being absent and more with a distractor in the rare versus frequent locations. These results support statistical learning of frequent distractor locations involving regional suppression in early visual cortex and point to differential neural mechanisms of distractor handling with different- versus same-dimension distractors.

3D Contrast Image Reconstruction From Human Brain Activity.

Several studies demonstrated that functional magnetic resonance imaging (fMRI) signals in early visual cortex can be used to reconstruct 2-dimensional (2D) visual contents. However, it remains unknown how to reconstruct 3-dimensional (3D) visual stimuli from fMRI signals in visual cortex. 3D visual stimuli contain 2D visual features and depth information. Moreover, binocular disparity is an important cue for depth perception. Thus, it is more challenging to reconstruct 3D visual stimuli than 2D visual stimuli from the fMRI signals of visual cortex. This study aimed to reconstruct 3D visual images by constructing three decoding models: contrast-decoding, disparity-decoding and contrast-disparity-decoding models, and testing these models with fMRI data from humans viewing 3D contrast images. The results revealed that the 3D contrast stimuli can be reconstructed from the visual cortex. And the early visual regions (V1, V2) showed predominant advantages in reconstructing the contrast in 3D images for the contrast-decoding model. The dorsal visual regions (V3A, V7 and MT) showed predominant advantages in decoding the disparity in 3D images for the disparity-decoding model. The combination of the early and dorsal visual regions showed predominant advantages in decoding both the contrast and disparity for the contrast-disparity-decoding model. The results suggested that the contrast and disparity in 3D images were mainly represented in the early and dorsal visual regions separately. The two visual systems may interact with each other to decode 3D-contrast images.

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-orderregions 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.

BOLD signal modulated with perception in the superficial layer of human V1 during binocular rivalry

During binocular rivalry, the alternation of the two eyes' percept correlates with the fluctuation of neural activities throughout the visual pathway, from as early as LGN and V1 to high-level occipital temporal visual cortices. However, it is not clear how feedforward and feedback processes interact to resolve the rivalrous inputs, and in particular, whether the observed neural fluctuations reflect feedforward, local or feedback modulations of resolved rivalry competition. To answer this question, we used ultra-high field fMRI at 7T with submillimeter resolution to measure rivalry-related signals from different layers of the human primary visual cortex, with the assumption that the middle layer is dominated by feedforward signals while feedback signals modulate the superficial and deep layers. BOLD signals in early visual cortex were acquired with T2*-weighted gradient echo EPI or T2-weighted balanced-SSFP pulse sequences. In the rivalry condition, a pair of orthogonal red and green gratings were dichoptically presented, and subjects reported their percept with button presses (red, green or mixed). In the replay condition, the same red/green gratings were monocularly presented in physical alternations to simulate the rivalry percept. The ocular dominance bias of V1 voxels was determined in separate scans using monocular checkerboard stimulus. Results show that in the replay condition, eye-specific modulation of BOLD signal was strongest in the middle (input) layer of V1; while in the rivalry condition, the rivalrous modulation of BOLD signal was strongest in the superficial layer. A transient signal was also observed, mainly from the superficial layer of V1, at the time points of perceptual transitions in the rivalry but not in the replay condition. These layer-specific fMRI findings support the idea that rivalry-related activity fluctuation in human primary visual cortex reflects feedback modulation from higher cortical areas. Meeting abstract presented at VSS 2018

Ultra-Rapid serial visual presentation reveals dynamics of feedforward and feedback processes in the ventral visual pathway.

Human visual recognition activates a dense network of overlapping feedforward and recurrent neuronal processes, making it hard to disentangle processing in the feedforward from the feedback direction. Here, we used ultra-rapid serial visual presentation to suppress sustained activity that blurs the boundaries of processing steps, enabling us to resolve two distinct stages of processing with MEG multivariate pattern classification. The first processing stage was the rapid activation cascade of the bottom-up sweep, which terminated early as visual stimuli were presented at progressively faster rates. The second stage was the emergence of categorical information with peak latency that shifted later in time with progressively faster stimulus presentations, indexing time-consuming recurrent processing. Using MEG-fMRI fusion with representational similarity, we localized recurrent signals in early visual cortex. Together, our findings segregated an initial bottom-up sweep from subsequent feedback processing, and revealed the neural signature of increased recurrent processing demands for challenging viewing conditions.

Laminar Organization of Working Memory Signals in Human Visual Cortex

The primary visual cortex (V1) not only represents incoming visual information but is also engaged by higher-level cognitive processes such as visual working memory. Given the laminar terminations of feedback connections between brain areas, such internally generated signals are thought to be present selectively in the deep and superficial layers of V1, and avoid the middle layers. Here, we provide empirical support for this notion, using lamina-resolved fMRI in humans. We observed item-specific working memory signals in early visual cortex. In V1, this item-specific activity was selectively present in deep and superficial layers, avoiding the middle layers, while working memory related activity was present in all layers of 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 separated.

Decoupling of BOLD amplitude and pattern classification of orientation-selective activity in human visual cortex

Multivariate pattern analysis (MVPA) of fMRI data has allowed the investigation of neural representations of stimuli on the basis of distributed patterns of activity within a brain region, independently from overall brain activity. For instance, several studies on early visual cortex have reported reliable MVPA decoding of the identity of a stimulus representation that was kept in working memory or internally generated, despite the fact that the overall BOLD response was low or even at baseline levels. Here we ask how it is possible that reliable stimulus information can be decoded from early visual cortex even when the overall BOLD signal remains low. We reanalyzed a data set in which human participants (N = 24) imagined or kept in working memory an oriented visual grating. We divided voxels from V1, V2, and V3 into groups based on orientation preference, and compared the time course of mean BOLD responses to preferred and non-preferred orientations with the time course of the multivariate decoding performance.Decoding accuracy related to a numerically small, but reliable univariate difference in the mean BOLD response to preferred and non-preferred stimuli. The time course of the difference in BOLD responses to preferred and non-preferred orientations was highly similar to the time course of the multivariate pattern classification accuracy. The reliability of the classification strongly correlated with the magnitude of differences in BOLD signal between preferred and non-preferred stimuli. These activity differences were small compared to the large overall BOLD modulations. This suggests that a substantial part of the task-related BOLD response to visual stimulation might not be stimulus-specific. Rather, stimulus-evoked BOLD signals in early visual cortex during a task context may be an amalgam of small stimulus-specific responses and large task-related but non-stimulus-specific responses. The latter are not evident during the maintenance or internal generation of stimulus representations, but provide an explanation of how reliable stimulus information can be decoded from early visual cortex even though its overall BOLD signal remains low.

Connectivity Reveals Sources of Predictive Coding Signals in Early Visual Cortex During Processing of Visual Optic Flow.

Superimposed on the visual feed-forward pathway, feedback connections convey higher level information to cortical areas lower in the hierarchy. A prominent framework for these connections is the theory of predictive coding where high-level areas send stimulus interpretations to lower level areas that compare them with sensory input. Along these lines, a growing body of neuroimaging studies shows that predictable stimuli lead to reduced blood oxygen level-dependent (BOLD) responses compared with matched nonpredictable counterparts, especially in early visual cortex (EVC) including areas V1-V3. The sources of these modulatory feedback signals are largely unknown. Here, we re-examined the robust finding of relative BOLD suppression in EVC evident during processing of coherent compared with random motion. Using functional connectivity analysis, we show an optic flow-dependent increase of functional connectivity between BOLD suppressed EVC and a network of visual motion areas including MST, V3A, V6, the cingulate sulcus visual area (CSv), and precuneus (Pc). Connectivity decreased between EVC and 2 areas known to encode heading direction: entorhinal cortex (EC) and retrosplenial cortex (RSC). Our results provide first evidence that BOLD suppression in EVC for predictable stimuli is indeed mediated by specific high-level areas, in accord with the theory of predictive coding.

Action preparation shapes processing in early visual cortex.

Preparation for an action, such as grasping an object, is accompanied by an enhanced perception of the object's action-relevant features, such as orientation and size. Cortical feedback from motor planning areas to early visual areas may drive this enhanced perception. To examine whether action preparation modulates activity in early human visual cortex, subjects grasped or pointed to oriented objects while high-resolution fMRI data were acquired. Using multivoxel pattern analysis techniques, we could decode with >70% accuracy whether a grasping or pointing action was prepared from signals in visual cortex as early as V1. These signals in early visual cortex were observed even when actions were only prepared but not executed. Anterior parietal cortex, on the other hand, showed clearest modulation for actual movements. This demonstrates that preparation of actions, even without execution, modulates relevant neuronal populations in early visual areas.

Perceptual learning in patients with macular degeneration.

Patients with age-related macular degeneration (AMD) or hereditary macular dystrophies (JMD) rely on an efficient use of their peripheral visual field. We trained eight AMD and five JMD patients to perform a texture-discrimination task (TDT) at their preferred retinal locus (PRL) used for fixation. Six training sessions of approximately one hour duration were conducted over a period of approximately 3 weeks. Before, during and after training twelve patients and twelve age-matched controls (the data from two controls had to be discarded later) took part in three functional magnetic resonance imaging (fMRI) sessions to assess training-related changes in the BOLD response in early visual cortex. Patients benefited from the training measurements as indexed by significant decrease (p = 0.001) in the stimulus onset asynchrony (SOA) between the presentation of the texture target on background and the visual mask, and in a significant location specific effect of the PRL with respect to hit rate (p = 0.014). The following trends were observed: (i) improvement in Vernier acuity for an eccentric line-bisection task; (ii) positive correlation between the development of BOLD signals in early visual cortex and initial fixation stability (r = 0.531); (iii) positive correlation between the increase in task performance and initial fixation stability (r = 0.730). The first two trends were non-significant, whereas the third trend was significant at p = 0.014, Bonferroni corrected. Consequently, our exploratory study suggests that training on the TDT can enhance eccentric vision in patients with central vision loss. This enhancement is accompanied by a modest alteration in the BOLD response in early visual cortex.

FEF-microstimulation causes task-dependent modulation of occipital fMRI activity

Electrical microstimulation of FEF (FEF-EM) modulates neuronal activity in area V4 (Moore and Armstrong, 2003) and elicits functional magnetic resonance imaging (fMRI) activations in visual cortex in a bottom-up dependent manner (Ekstrom et al., 2008). Here we test the hypothesis that FEF-EM-induced modulations of fMRI activity are also function of task demands, which would suggest top-down dependent gating of FEF signals in early visual cortex. We scanned two monkeys performing a visually guided saccade task; a passive fixation task with a very similar visual display; and a passive fixation task without peripheral dots. We found increased effects of FEF-EM on fMRI-activity in visual cortex during saccades compared to fixation, indicating that the FEF-EM induced modulation is task-dependent. Finally, the effect of FEF-EM is mainly present in voxels which were less activated by visual stimuli in the absence of electrical stimulation. Our results show that the FEF-EM-induced pattern of activation in early visual cortex is topographically specific and more pronounced during increased task demands. These results fit with models suggesting that FEF is an important source modulating activity in early sensory cortex and that these influences can be enhanced by coincident bottom-up or top-down signals.

Behavioral Effects of Electrical Microstimulation in FEF of the Macaque Monkey with chronically implanted wire electrodes

Behavioral Effects of Electrical Microstimulation in FEF of the Macaque Monkey with chronically implanted wire electrodes

Decoding Successive Computational Stages of Saliency Processing

An important requirement for vision is to identify interesting and relevant regions of the environment for further processing. Some models assume that salient locations from a visual scene are encoded in a dedicated spatial saliency map [1, 2]. Then, a winner-take-all (WTA) mechanism [1, 2] is often believed to threshold the graded saliency representation and identify the most salient position in the visual field. Here we aimed to assess whether neural representations of graded saliency and the subsequent WTA mechanism can be dissociated. We presented images of natural scenes while subjects were in a scanner performing a demanding fixation task, and thus their attention was directed away. Signals in early visual cortex and posterior intraparietal sulcus (IPS) correlated with graded saliency as defined by a computational saliency model. Multivariate pattern classification [3, 4] revealed that the most salient position in the visual field was encoded in anterior IPS and frontal eye fields (FEF), thus reflecting a potential WTA stage. Our results thus confirm that graded saliency and WTA-thresholded saliency are encoded in distinct neural structures. This could provide the neural representation required for rapid and automatic orientation toward salient events in natural environments.

Distribution of attention modulates salience signals in early visual cortex.

Previous research has shown that the extent to which people spread attention across the visual field plays a crucial role in visual selection and the occurrence of bottom-up driven attentional capture. Consistent with previous findings, we show that when attention was diffusely distributed across the visual field while searching for a shape singleton, an irrelevant salient color singleton captured attention. However, while using the very same displays and task, no capture was observed when observers initially focused their attention at the center of the display. Using event-related fMRI, we examined the modulation of retinotopic activity related to attentional capture in early visual areas. Because the sensory display characteristics were identical in both conditions, we were able to isolate the brain activity associated with exogenous attentional capture. The results show that spreading of attention leads to increased bottom-up exogenous capture and increased activity in visual area V3 but not in V2 and V1.

Perceptual Learning Increases the Strength of the Earliest Signals in Visual Cortex

Training improves performance on most visual tasks. Such perceptual learning can modify how information is read out from, and represented in, later visual areas, but effects on early visual cortex are controversial. In particular, it remains unknown whether learning can reshape neural response properties in early visual areas independent from feedback arising in later cortical areas. Here, we tested whether learning can modify feedforward signals in early visual cortex as measured by the human electroencephalogram. Fourteen subjects were trained for >24 d to detect a diagonal grating pattern in one quadrant of the visual field. Training improved performance, reducing the contrast needed for reliable detection, and also reliably increased the amplitude of the earliest component of the visual evoked potential, the C1. Control orientations and locations showed smaller effects of training. Because the C1 arises rapidly and has a source in early visual cortex, our results suggest that learning can increase early visual area response through local receptive field changes without feedback from later areas.

Retinotopic Coding of Extraretinal Pursuit Signals in Early Visual Cortex

During smooth pursuit, the image of the target is stabilized on the fovea, implying that speed judgments made during pursuit must rely on an extraretinal signal providing precise eye speed information. To characterize the introduction of such extraretinal signal into the human visual system, we performed a factorial, functional magnetic resonance imaging experiment, in which we manipulated the factor eye movement, with "fixation" and "pursuit" as levels, and the factor task, with "speed" and "form" judgments as levels. We hypothesized that the extraretinal speed signal is reflected as an interaction between speed judgments and pursuit. Random effects analysis yielded an interaction only in dorsal early visual cortex. Retinotopic mapping localized this interaction on the horizontal meridian (HM) between dorsal areas visual 2 and 3 (V2/V3) at 1-2 degrees azimuth. This corresponded to the position the pursuit target would have reached, if moving retinotopically, at the time of the subject's speed judgment. Because the 2 V2/V3 HMs are redundant, both may be involved in speed judgments, the ventral one involving judgments based on retinal motion and the dorsal one judgments requiring an internal signal. These results indicate that an extraretinal speed signal is injected into early visual cortex during pursuit.

Bayesian belief propagation and border-ownership signals in early visual cortex

Bayesian belief propagation and border-ownership signals in early visual cortex

Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex

The frontal eye field (FEF) is one of several cortical regions thought to modulate sensory inputs. Moreover, several hypotheses suggest that the FEF can only modulate early visual areas in the presence of a visual stimulus. To test for bottom-up gating of frontal signals, we microstimulated subregions in the FEF of two monkeys and measured the effects throughout the brain with functional magnetic resonance imaging. The activity of higher-order visual areas was strongly modulated by FEF stimulation, independent of visual stimulation. In contrast, FEF stimulation induced a topographically specific pattern of enhancement and suppression in early visual areas, but only in the presence of a visual stimulus. Modulation strength depended on stimulus contrast and on the presence of distractors. We conclude that bottom-up activation is needed to enable top-down modulation of early visual cortex and that stimulus saliency determines the strength of this modulation.