Area V1 Research Articles

Spatiotopic Adaptation in Visual Areas.

The ability to perceive the visual world around us as spatially stable despite frequent eye movements is one of the long-standing mysteries of neuroscience. The existence of neural mechanisms processing spatiotopic information is indispensable for a successful interaction with the external world. However, how the brain handles spatiotopic information remains a matter of debate. We here combined behavioral and fMRI adaptation to investigate the coding of spatiotopic information in the human brain. Subjects were adapted by a prolonged presentation of a tilted grating. Thereafter, they performed a saccade followed by the brief presentation of a probe. This procedure allowed dissociating adaptation aftereffects at retinal and spatiotopic positions. We found significant behavioral and functional adaptation in both retinal and spatiotopic positions, indicating information transfer into a spatiotopic coordinate system. The brain regions involved were located in ventral visual areas V3, V4, and VO. Our findings suggest that spatiotopic representations involved in maintaining visual stability are constructed by dynamically remapping visual feature information between retinotopic regions within early visual areas. Why do we perceive the visual world as stable, although we constantly perform saccadic eye movements? We investigated how the visual system codes object locations in spatiotopic (i.e., external world) coordinates. We combined visual adaptation, in which the prolonged exposure to a specific visual feature alters perception, with fMRI adaptation, where the repeated presentation of a stimulus leads to a reduction in the BOLD amplitude. Functionally, adaptation was found in visual areas representing the retinal location of an adaptor but also at representations corresponding to its spatiotopic position. The results suggest that an active dynamic shift transports information in visual cortex to counteract the retinal displacement associated with saccade eye movements.

Distinct fMRI Responses to Self-Induced versus Stimulus Motion during Free Viewing in the Macaque

Visual motion responses in the brain are shaped by two distinct sources: the physical movement of objects in the environment and motion resulting from one's own actions. The latter source, termed visual reafference, stems from movements of the head and body, and in primates from the frequent saccadic eye movements that mark natural vision. To study the relative contribution of reafferent and stimulus motion during natural vision, we measured fMRI activity in the brains of two macaques as they freely viewed >50 hours of naturalistic video footage depicting dynamic social interactions. We used eye movements obtained during scanning to estimate the level of reafferent retinal motion at each moment in time. We also estimated the net stimulus motion by analyzing the video content during the same time periods. Mapping the responses to these distinct sources of retinal motion, we found a striking dissociation in the distribution of visual responses throughout the brain. Reafferent motion drove fMRI activity in the early retinotopic areas V1, V2, V3, and V4, particularly in their central visual field representations, as well as lateral aspects of the caudal inferotemporal cortex (area TEO). However, stimulus motion dominated fMRI responses in the superior temporal sulcus, including areas MT, MST, and FST as well as more rostral areas. We discuss this pronounced separation of motion processing in the context of natural vision, saccadic suppression, and the brain's utilization of corollary discharge signals. Visual motion arises not only from events in the external world, but also from the movements of the observer. For example, even if objects are stationary in the world, the act of walking through a room or shifting one's eyes causes motion on the retina. This "reafferent" motion propagates into the brain as signals that must be interpreted in the context of real object motion. The delineation of whole-brain responses to stimulus versus self-generated retinal motion signals is critical for understanding visual perception and is of pragmatic importance given the increasing use of naturalistic viewing paradigms. The present study uses fMRI to demonstrate that the brain exhibits a fundamentally different pattern of responses to these two sources of retinal motion.

Eye-position signals in the local field potentials of area V1

Eye-position signals in the local field potentials of area V1

Mechanisms of Saccadic Suppression in Primate Cortical Area V4.

Psychophysical studies have shown that subjects are often unaware of visual stimuli presented around the time of an eye movement. This saccadic suppression is thought to be a mechanism for maintaining perceptual stability. The brain might accomplish saccadic suppression by reducing the gain of visual responses to specific stimuli or by simply suppressing firing uniformly for all stimuli. Moreover, the suppression might be identical across the visual field or concentrated at specific points. To evaluate these possibilities, we recorded from individual neurons in cortical area V4 of nonhuman primates trained to execute saccadic eye movements. We found that both modes of suppression were evident in the visual responses of these neurons and that the two modes showed different spatial and temporal profiles: while gain changes started earlier and were more widely distributed across visual space, nonspecific suppression was found more often in the peripheral visual field, after the completion of the saccade. Peripheral suppression was also associated with increased noise correlations and stronger local field potential oscillations in the α frequency band. This pattern of results suggests that saccadic suppression shares some of the circuitry responsible for allocating voluntary attention. We explore our surroundings by looking at things, but each eye movement that we make causes an abrupt shift of the visual input. Why doesn't the world look like a film recorded on a shaky camera? The answer in part is a brain mechanism called saccadic suppression, which reduces the responses of visual neurons around the time of each eye movement. Here we reveal several new properties of the underlying mechanisms. First, the suppression operates differently in the central and peripheral visual fields. Second, it appears to be controlled by oscillations in the local field potentials at frequencies traditionally associated with attention. These results suggest that saccadic suppression shares the brain circuits responsible for actively ignoring irrelevant stimuli.

Ongoing Slow Fluctuations in V1 Impact on Visual Perception.

The human brain’s ongoing activity is characterized by intrinsic networks of coherent fluctuations, measured for example with correlated functional magnetic resonance imaging signals. So far, however, the brain processes underlying this ongoing blood oxygenation level dependent (BOLD) signal orchestration and their direct relevance for human behavior are not sufficiently understood. In this study, we address the question of whether and how ongoing BOLD activity within intrinsic occipital networks impacts on conscious visual perception. To this end, backwardly masked targets were presented in participants’ left visual field only, leaving the ipsi-lateral occipital areas entirely free from direct effects of task throughout the experiment. Signal time courses of ipsi-lateral BOLD fluctuations in visual areas V1 and V2 were then used as proxies for the ongoing contra-lateral BOLD activity within the bilateral networks. Magnitude and phase of these fluctuations were compared in trials with and without conscious visual perception, operationalized by means of subjective confidence ratings. Our results show that ipsi-lateral BOLD magnitudes in V1 were significantly higher at times of peak response when the target was perceived consciously. A significant difference between conscious and non-conscious perception with regard to the pre-target phase of an intrinsic-frequency regime suggests that ongoing V1 fluctuations exert a decisive impact on the access to consciousness already before stimulation. Both effects were absent in V2. These results thus support the notion that ongoing slow BOLD activity within intrinsic networks covering V1 represents localized processes that modulate the degree of readiness for the emergence of visual consciousness.

How Invariant Feature Selectivity Is Achieved in Cortex.

Parsing the visual scene into objects is paramount to survival. Yet, how this is accomplished by the nervous system remains largely unknown, even in the comparatively well understood visual system. It is especially unclear how detailed peripheral signal representations are transformed into the object-oriented representations that are independent of object position and are provided by the final stages of visual processing. This perspective discusses advances in computational algorithms for fitting large-scale models that make it possible to reconstruct the intermediate steps of visual processing based on neural responses to natural stimuli. In particular, it is now possible to characterize how different types of position invariance, such as local (also known as phase invariance) and more global, are interleaved with nonlinear operations to allow for coding of curved contours. Neurons in the mid-level visual area V4 exhibit selectivity to pairs of even- and odd-symmetric profiles along curved contours. Such pairing is reminiscent of the response properties of complex cells in the primary visual cortex (V1) and suggests specific ways in which V1 signals are transformed within subsequent visual cortical areas. These examples illustrate that large-scale models fitted to neural responses to natural stimuli can provide generative models of successive stages of sensory processing.

Attention operates uniformly throughout the classical receptive field and the surround.

Shifting attention among visual stimuli at different locations modulates neuronal responses in heterogeneous ways, depending on where those stimuli lie within the receptive fields of neurons. Yet how attention interacts with the receptive-field structure of cortical neurons remains unclear. We measured neuronal responses in area V4 while monkeys shifted their attention among stimuli placed in different locations within and around neuronal receptive fields. We found that attention interacts uniformly with the spatially-varying excitation and suppression associated with the receptive field. This interaction explained the large variability in attention modulation across neurons, and a non-additive relationship among stimulus selectivity, stimulus-induced suppression and attention modulation that has not been previously described. A spatially-tuned normalization model precisely accounted for all observed attention modulations and for the spatial summation properties of neurons. These results provide a unified account of spatial summation and attention-related modulation across both the classical receptive field and the surround.

Texture Segregation Causes Early Figure Enhancement and Later Ground Suppression in Areas V1 and V4 of Visual Cortex.

Segregation of images into figures and background is fundamental for visual perception. Cortical neurons respond more strongly to figural image elements than to background elements, but the mechanisms of figure–ground modulation (FGM) are only partially understood. It is unclear whether FGM in early and mid-level visual cortex is caused by an enhanced response to the figure, a suppressed response to the background, or both.We studied neuronal activity in areas V1 and V4 in monkeys performing a texture segregation task. We compared texture-defined figures with homogeneous textures and found an early enhancement of the figure representation, and a later suppression of the background. Across neurons, the strength of figure enhancement was independent of the strength of background suppression.We also examined activity in the different V1 layers. Both figure enhancement and ground suppression were strongest in superficial and deep layers and weaker in layer 4. The current–source density profiles suggested that figure enhancement was caused by stronger synaptic inputs in feedback-recipient layers 1, 2, and 5 and ground suppression by weaker inputs in these layers, suggesting an important role for feedback connections from higher level areas. These results provide new insights into the mechanisms for figure–ground organization.

Absolute Depth Sensitivity in Cat Primary Visual Cortex under Natural Viewing Conditions.

Mechanisms of 3D perception, investigated in many laboratories, have defined depth either relative to the fixation plane or to other objects in the visual scene. It is obvious that for efficient perception of the 3D world, additional mechanisms of depth constancy could operate in the visual system to provide information about absolute distance. Neurons with properties reflecting some features of depth constancy have been described in the parietal and extrastriate occipital cortical areas. It has also been shown that, for some neurons in the visual area V1, responses to stimuli of constant angular size differ at close and remote distances. The present study was designed to investigate whether, in natural free gaze viewing conditions, neurons tuned to absolute depths can be found in the primary visual cortex (area V1). Single-unit extracellular activity was recorded from the visual cortex of waking cats sitting on a trolley in front of a large screen. The trolley was slowly approaching the visual scene, which consisted of stationary sinusoidal gratings of optimal orientation rear-projected over the whole surface of the screen. Each neuron was tested with two gratings, with spatial frequency of one grating being twice as high as that of the other. Assuming that a cell is tuned to a spatial frequency, its maximum response to the grating with a spatial frequency twice as high should be shifted to a distance half way closer to the screen in order to attain the same size of retinal projection. For hypothetical neurons selective to absolute depth, location of the maximum response should remain at the same distance irrespective of the type of stimulus. It was found that about 20% of neurons in our experimental paradigm demonstrated sensitivity to particular distances independently of the spatial frequencies of the gratings. We interpret these findings as an indication of the use of absolute depth information in the primary visual cortex.

Neurons in Macaque Area V4 Are Tuned for Complex Spatio-Temporal Patterns

To deepen our understanding of object recognition, it is critical to understand the nature of transformations that occur in intermediate stages of processing in the ventral visual pathway, such as area V4. Neurons in V4 are selective to local features of global shape, such as extended contours. Previously, we found that V4 neurons selective for curved elements exhibit a high degree of spatial variation in their preference. If spatial variation in curvature selectivity was also marked by distinct temporal response patterns at different spatial locations, then it might be possible to untangle this information in subsequent processing based on temporal responses. Indeed, we find that V4 neurons whose receptive fields exhibit intricate selectivity also show variation in their temporal responses across locations. A computational model that decodes stimulus identity based on population responses benefits from using this temporal information, suggesting that it could provide a multiplexed code for spatio-temporal features.

Neural Computation of Surface Border Ownership and Relative Surface Depth from Ambiguous Contrast Inputs.

The segregation of image parts into foreground and background is an important aspect of the neural computation of 3D scene perception. To achieve such segregation, the brain needs information about border ownership; that is, the belongingness of a contour to a specific surface represented in the image. This article presents psychophysical data derived from 3D percepts of figure and ground that were generated by presenting 2D images composed of spatially disjoint shapes that pointed inward or outward relative to the continuous boundaries that they induced along their collinear edges. The shapes in some images had the same contrast (black or white) with respect to the background gray. Other images included opposite contrasts along each induced continuous boundary. Psychophysical results demonstrate conditions under which figure-ground judgment probabilities in response to these ambiguous displays are determined by the orientation of contrasts only, not by their relative contrasts, despite the fact that many border ownership cells in cortical area V2 respond to a preferred relative contrast. Studies are also reviewed in which both polarity-specific and polarity-invariant properties obtain. The FACADE and 3D LAMINART models are used to explain these data.

Dynamics of excitatory and inhibitory networks are differentially altered by selective attention.

Inhibition and excitation form two fundamental modes of neuronal interaction, yet we understand relatively little about their distinct roles in service of perceptual and cognitive processes. We developed a multidimensional waveform analysis to identify fast-spiking (putative inhibitory) and regular-spiking (putative excitatory) neurons in vivo and used this method to analyze how attention affects these two cell classes in visual area V4 of the extrastriate cortex of rhesus macaques. We found that putative inhibitory neurons had both greater increases in firing rate and decreases in correlated variability with attention compared with putative excitatory neurons. Moreover, the time course of attention effects for putative inhibitory neurons more closely tracked the temporal statistics of target probability in our task. Finally, the session-to-session variability in a behavioral measure of attention covaried with the magnitude of this effect. Together, these results suggest that selective targeting of inhibitory neurons and networks is a critical mechanism for attentional modulation.

Spike synchrony generated by modulatory common input through NMDA-type synapses.

Common excitatory input to neurons increases their firing rates and the strength of the spike correlation (synchrony) between them. Little is known, however, about the synchronizing effects of modulatory common input. Here, we show that modulatory common input with the slow synaptic kinetics of N-methyl-d-aspartate (NMDA) receptors enhances firing rates and also produces synchrony. Tight synchrony (correlations on the order of milliseconds) always increases with modulatory strength. Unexpectedly, the relationship between strength of modulation and strength of loose synchrony (tens of milliseconds) is not monotonic: The strongest loose synchrony is obtained for intermediate modulatory amplitudes. This finding explains recent neurophysiological results showing that in cortical areas V1 and V2, presumed modulatory top-down input due to contour grouping increases (loose and tight) synchrony but that additional modulatory input due to top-down attention does not change tight synchrony and actually decreases loose synchrony. These neurophysiological findings are understood from our model of integrate-and-fire neurons under the assumption that contour grouping as well as attention lead to additive modulatory common input through NMDA-type synapses. In contrast, circuits with common projections through model α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors did not exhibit the paradoxical decrease of synchrony with increased input. Our results suggest that NMDA receptors play a critical role in top-down response modulation in the visual cortex.

Low-level mediation of directionally specific motion aftereffects: Motion perception is not necessary

Previous psychophysical experiments with normal human observers have shown that adaptation to a moving dot stream causes directionally specific repulsion in the perceived angle of a subsequently viewed moving probe. In this study, we used a two-alternative forced choice task with roving pedestals to determine the conditions that are necessary and sufficient for producing directionally specific repulsion with compound adaptors, each of which contains two oppositely moving, differently colored component streams. Experiment 1 provided a demonstration of repulsion between single-component adaptors and probes moving at approximately 90° or 270°. In Experiment 2, oppositely moving dots in the adaptor were paired to preclude the appearance of motion. Nonetheless, repulsion remained strong when the angle between each probe stream and one component was approximately 30°. In Experiment 3, adapting dot pairs were kept stationary during their limited lifetimes. Their orientation content alone proved insufficient for producing repulsion. In Experiments 4–6, the angle between the probe and both adapting components was approximately 90° or 270°. Directional repulsion was found when observers were asked to visually track one of the adapting components (Exp. 6), but not when they were asked to attentionally track it (Exp. 5), nor while they passively viewed the adaptor (Exp. 4). Our results are consistent with a low-level mechanism for motion adaptation. This mechanism is not selective for stimulus color and is not susceptible to attentional modulation. The most likely cortical locus of adaptation is area V1.Electronic supplementary materialThe online version of this article (doi:10.3758/s13414-016-1160-1) contains supplementary material, which is available to authorized users.

Global Motion Processing in Human Visual Cortical Areas V2 and V3.

Global motion perception entails the ability to extract the central direction tendency from an extended area of visual space containing widely disparate local directions. A substantial body of evidence suggests that local motion signals generated in primary visual cortex (V1) are spatially integrated to provide perception of global motion, beginning in the middle temporal area (MT) in macaques and its counterpart in humans, hMT. However, V2 and V3 also contain motion-sensitive neurons that have larger receptive fields than those found in V1, giving the potential for spatial integration of motion signals. Despite this, V2 and V3 have been overlooked as sites of global motion processing. To test, free of local-global confounds, whether human V2 and V3 are important for encoding global motion, we developed a visual stimulus that yields a global direction yet includes all possible local directions and is perfectly balanced at the local motion level. We then attempted to decode global motion direction in such stimuli with multivariate pattern classification of fMRI data. We found strong sensitivity to global motion in hMT, as expected, and also in several higher visual areas known to encode optic flow. Crucially, we found that global motion direction could be decoded in human V2 and, particularly, in V3. The results suggest the surprising conclusion that global motion processing is a key function of cortical visual areas V2 and V3. A possible purpose is to provide global motion signals to V6. Humans can readily detect the overall direction of movement in a flock of birds despite large differences in the directions of individual birds at a given moment. This ability to combine disparate motion signals across space underlies many aspects of visual motion perception and has therefore received considerable research attention. The received wisdom is that spatial integration of motion signals occurs in the cortical motion complex MT+ in both human and nonhuman primates. We show here that areas V2 and V3 in humans are also able to perform this function. We suggest that different cortical areas integrate motion signals in different ways for different purposes.

Gamma Frequency and the Spatial Tuning of Primary Visual Cortex.

Visual stimulation produces oscillatory gamma responses in human primary visual cortex (V1) that also relate to visual perception. We have shown previously that peak gamma frequency positively correlates with central V1 cortical surface area. We hypothesized that people with larger V1 would have smaller receptive fields and that receptive field size, not V1 area, might explain this relationship. Here we set out to test this hypothesis directly by investigating the relationship between fMRI estimated population receptive field (pRF) size and gamma frequency in V1. We stimulated both the near-center and periphery of the visual field using both large and small stimuli in each location and replicated our previous finding of a positive correlation between V1 surface area and peak gamma frequency. Counter to our expectation, we found that between participants V1 size (and not PRF size) accounted for most of the variability in gamma frequency. Within-participants we found that gamma frequency increased, rather than decreased, with stimulus eccentricity directly contradicting our initial hypothesis.

Responses in early visual areas to contour integration are context dependent.

It has been shown that early visual areas are involved in contour processing. However, it is not clear how local and global context interact to influence responses in those areas, nor has the interarea coordination that yields coherent structural percepts been fully studied, especially in human observers. In this study, we used functional magnetic resonance imaging (fMRI) to measure activity in early visual cortex while observers performed a contour detection task in which alignment of Gabor elements and background clutter were manipulated. Six regions of interest (two regions, containing either the cortex representing the target or the background clutter, in each of areas V1, V2, and V3) were predefined using separate target versus background functional localizer scans. The first analysis using a general linear model showed that in the presence of background clutter, responses in V1 and V2 target regions of interest were significantly stronger to aligned than unaligned contours, whereas when background clutter was absent, no significant difference was observed. The second analysis using interarea correlations showed that with background clutter, there was an increase in V1–V2 coordination within the target regions when perceiving aligned versus unaligned contours; without clutter, however, correlations between V1 and V2 were similar no matter whether aligned contours were present or not. Both the average response magnitude and the connectivity analysis suggest different mechanisms support contour processing with or without background distractors. Coordination between V1 and V2 may play a major role in coherent structure perception, especially with complex scene organization.

A Biologically Inspired Appearance Model for Robust Visual Tracking.

In this paper, we propose a biologically inspired appearance model for robust visual tracking. Motivated in part by the success of the hierarchical organization of the primary visual cortex (area V1), we establish an architecture consisting of five layers: whitening, rectification, normalization, coding, and pooling. The first three layers stem from the models developed for object recognition. In this paper, our attention focuses on the coding and pooling layers. In particular, we use a discriminative sparse coding method in the coding layer along with spatial pyramid representation in the pooling layer, which makes it easier to distinguish the target to be tracked from its background in the presence of appearance variations. An extensive experimental study shows that the proposed method has higher tracking accuracy than several state-of-the-art trackers.

Competitive Dynamics in MSTd: A Mechanism for Robust Heading Perception Based on Optic Flow.

Human heading perception based on optic flow is not only accurate, it is also remarkably robust and stable. These qualities are especially apparent when observers move through environments containing other moving objects, which introduce optic flow that is inconsistent with observer self-motion and therefore uninformative about heading direction. Moving objects may also occupy large portions of the visual field and occlude regions of the background optic flow that are most informative about heading perception. The fact that heading perception is biased by no more than a few degrees under such conditions attests to the robustness of the visual system and warrants further investigation. The aim of the present study was to investigate whether recurrent, competitive dynamics among MSTd neurons that serve to reduce uncertainty about heading over time offer a plausible mechanism for capturing the robustness of human heading perception. Simulations of existing heading models that do not contain competitive dynamics yield heading estimates that are far more erratic and unstable than human judgments. We present a dynamical model of primate visual areas V1, MT, and MSTd based on that of Layton, Mingolla, and Browning that is similar to the other models, except that the model includes recurrent interactions among model MSTd neurons. Competitive dynamics stabilize the model’s heading estimate over time, even when a moving object crosses the future path. Soft winner-take-all dynamics enhance units that code a heading direction consistent with the time history and suppress responses to transient changes to the optic flow field. Our findings support recurrent competitive temporal dynamics as a crucial mechanism underlying the robustness and stability of perception of heading.

Multiple asynchronous stimulus- and task-dependent hierarchies (STDH) within the visual brain's parallel processing systems.

Results from a variety of sources, some many years old, lead ineluctably to a re-appraisal of the twin strategies of hierarchical and parallel processing used by the brain to construct an image of the visual world. Contrary to common supposition, there are at least three 'feed-forward' anatomical hierarchies that reach the primary visual cortex (V1) and the specialized visual areas outside it, in parallel. These anatomical hierarchies do not conform to the temporal order with which visual signals reach the specialized visual areas through V1. Furthermore, neither the anatomical hierarchies nor the temporal order of activation through V1 predict the perceptual hierarchies. The latter shows that we see (and become aware of) different visual attributes at different times, with colour leading form (orientation) and directional visual motion, even though signals from fast-moving, high-contrast stimuli are among the earliest to reach the visual cortex (of area V5). Parallel processing, on the other hand, is much more ubiquitous than commonly supposed but is subject to a barely noticed but fundamental aspect of brain operations, namely that different parallel systems operate asynchronously with respect to each other and reach perceptual endpoints at different times. This re-assessment leads to the conclusion that the visual brain is constituted of multiple, parallel and asynchronously operating task- and stimulus-dependent hierarchies (STDH); which of these parallel anatomical hierarchies have temporal and perceptual precedence at any given moment is stimulus and task related, and dependent on the visual brain's ability to undertake multiple operations asynchronously.