Cross-orientation Suppression Research Articles

Investigating cross-orientation inhibition with continuous tracking.

We investigated cross-orientation inhibition with the recently developed continuous tracking technique. We designed an experiment where participants tracked the horizontal motion of a narrow vertical grating. The target was superimposed on one of three different backgrounds, in separate sessions: a uniform gray background or a sinusoidal grating oriented either parallel or orthogonal to the target. Both mask and target where phase reversed. We cross-correlated target and mouse movements and compared the peaks and lags of response with the different masks. Our results are in agreement with previous findings on cross-orientation inhibition: The orthogonal mask had a weak effect on the peaks and lags of correlation as a function of target contrast, consistently with a divisive effect of the mask, while the parallel mask acted subtractively on the response. Interestingly, lags of correlation decreased approximately linearly with contrast, with decrements of the order of 100ms, even at 10 times the detection threshold, confirming that it is possible to investigate behavioral differences above threshold using the continuous tracking paradigm.

No Evidence of Cross-Orientation Suppression Differences in Migraine with Aura Compared to Healthy Controls.

It has been suggested that there may be an imbalance of excitation and inhibitory processes in the visual areas of the brain in people with migraine aura (MA). One idea is thalamocortical dysrhythmia, characterized by disordered oscillations, and thus disordered communication between the lateral geniculate nucleus and the cortex. Cross-orientation suppression is a visual task thought to rely on inhibitory processing, possibly originating in the lateral geniculate nucleus. We measured both resting-state oscillations and cross-orientation suppression using EEG over occipital areas in people with MA and healthy volunteers. We found evidence of cross-orientation suppression in the SSVEP responses, but no evidence of any group difference. Therefore, inhibitory processes related to cross-orientation suppression do not appear to be impaired in MA.

Mechanism underpinning the sharpening of orientation and spatial frequency selectivities in the tree shrew (Tupaia belangeri) primary visual cortex.

Most neurons in the primary visual cortex (V1) of mammals show sharp orientation selectivity and band-pass spatial frequency tuning. Here, we examine whether sharpening of the broad tuning that exists subcortically, namely in the retina and the lateral geniculate nucleus (LGN), underlie the sharper tuning seen for both the above features in tree shrew V1. Since the transition from poor feature selectivity to sharp tuning occurs entirely within V1 in tree shrews, we examined the orientation selectivity and spatial frequency tuning of neurons within individual electrode penetrations. We found that most layer 4 and layer 2/3 neurons in the same cortical column preferred the same stimulus orientation. However, a subset of layer 3c neurons close to the layer 4 border preferred near orthogonal orientations, suggesting that layer 2/3 neurons may inherit the orientation preferences of their layer 4 input neurons and also receive cross-orientation inhibition from layer 3c neurons. We also found that layer 4 neurons showed sharper orientation selectivity at higher spatial frequencies, suggesting that attenuation of low spatial frequency responses by spatially broad inhibition acting on layer 4 inputs to layer 2/3 neurons can enhance both orientation and spatial frequency selectivities. However, in a proportion of layer 2/3 neurons, the sharper tuning of layer 2/3 neurons appeared to arise also or even mainly from inhibition specific to high spatial frequencies acting on the layer 4 inputs to layer 2/3. Overall, our results are consistent with the suggestion that in tree shrews, sharp feature selectivity in layer 2/3 can be established by intracortical mechanisms that sharpen biases observed in layer 4, which are in turn inherited presumably from thalamic afferents.

Steady-state measures of visual suppression.

In the early visual system, suppression occurs between neurons representing different stimulus properties. This includes features such as orientation (cross-orientation suppression), eye-of-origin (interocular suppression) and spatial location (surround suppression), which are thought to involve distinct anatomical pathways. We asked if these separate routes to suppression can be differentiated by their pattern of gain control on the contrast response function measured in human participants using steady-state electroencephalography. Changes in contrast gain shift the contrast response function laterally, whereas changes in response gain scale the function vertically. We used a Bayesian hierarchical model to summarise the evidence for each type of gain control. A computational meta-analysis of 16 previous studies found the most evidence for contrast gain effects with overlaid masks, but no clear evidence favouring either response gain or contrast gain for other mask types. We then conducted two new experiments, comparing suppression from four mask types (monocular and dichoptic overlay masks, and aligned and orthogonal surround masks) on responses to sine wave grating patches flickering at 5Hz. At the occipital pole, there was strong evidence for contrast gain effects in all four mask types at the first harmonic frequency (5Hz). Suppression generally became stronger at more lateral electrode sites, but there was little evidence of response gain effects. At the second harmonic frequency (10Hz) suppression was stronger overall, and involved both contrast and response gain effects. Although suppression from different mask types involves distinct anatomical pathways, gain control processes appear to serve a common purpose, which we suggest might be to suppress less reliable inputs.

Plaid Detectors in Macaque V1 Revealed by Two-Photon Calcium Imaging.

Neuronal responses to one-dimensional orientations are combined to represent two-dimensional composite patterns; this plays a key role in intermediate-level vision such as texture segmentation. However, where and how the visual cortex starts to represent composite patterns, such as a plaid consisting of two superimposing gratings of different orientations, remains neurophysiologically elusive. Psychophysical and modeling evidence has suggested the existence of early neural mechanisms specialized in plaid detection [1-6], but the responses of V1 neurons to an optimally orientated grating are actually suppressed by a superimposing grating of different orientation (i.e., cross-orientation inhibition) [7, 8]. Would some other V1 neurons be plaid detectors? Here, we used two-photon calcium imaging [9] to compare the responses of V1 superficial-layer neurons to gratings and plaids in awake macaques. We found that many non-orientation-tuned neurons responded weakly to gratings but strongly to plaids, often with plaid orientation selectivity and cross-angle selectivity. In comparison, most (∼94%) orientation-tuned neurons showed more or less cross-orientation inhibition, regardless of the relative stimulus contrasts. Only a small portion (∼8%) of them showed plaid facilitation at off-peak orientations. These results suggest separate subpopulations of plaid and grating responding neurons. Because most of these plaid neurons (∼95%) were insensitive to motion direction, they were plaid pattern detectors, not plaid motion detectors.

Temporal Contingencies Determine Whether Adaptation Strengthens or Weakens Normalization.

A fundamental and nearly ubiquitous feature of sensory encoding is that neuronal responses are strongly influenced by recent experience, or adaptation. Theoretical and computational studies have proposed that many adaptation effects may result in part from changes in the strength of normalization signals. Normalization is a "canonical" computation in which a neuron's response is modulated (normalized) by the pooled activity of other neurons. Here, we test whether adaptation can alter the strength of cross-orientation suppression, or masking, a paradigmatic form of normalization evident in primary visual cortex (V1). We made extracellular recordings of V1 neurons in anesthetized male macaques and measured responses to plaid stimuli composed of two overlapping, orthogonal gratings before and after prolonged exposure to two distinct adapters. The first adapter was a plaid consisting of orthogonal gratings and led to stronger masking. The second adapter presented the same orthogonal gratings in an interleaved manner and led to weaker masking. The strength of adaptation's effects on masking depended on the orientation of the test stimuli relative to the orientation of the adapters, but was independent of neuronal orientation preference. Changes in masking could not be explained by altered neuronal responsivity. Our results suggest that normalization signals can be strengthened or weakened by adaptation depending on the temporal contingencies of the adapting stimuli. Our findings reveal an interplay between two widespread computations in cortical circuits, adaptation and normalization, that enables flexible adjustments to the structure of the environment, including the temporal relationships among sensory stimuli.SIGNIFICANCE STATEMENT Two fundamental features of sensory responses are that they are influenced by adaptation and that they are modulated by the activity of other nearby neurons via normalization. Our findings reveal a strong interaction between these two aspects of cortical computation. Specifically, we show that cross-orientation masking, a form of normalization, can be strengthened or weakened by adaptation depending on the temporal contingencies between sensory inputs. Our findings support theoretical proposals that some adaptation effects may involve altered normalization and offer a network-based explanation for how cortex adjusts to current sensory demands.

Characterizing Non-Linear Processes in Cross-Orientation Suppression (XOS) with Steady-State Visual Evoked Potentials (SSVEPs)

Characterizing Non-Linear Processes in Cross-Orientation Suppression (XOS) with Steady-State Visual Evoked Potentials (SSVEPs)

Intact perceptual bias in autism contradicts the decreased normalization model

One recent, promising account of Autism Spectrum Disorders (ASD) situates the cause of the disorder in an atypicality in basic neural information processing, more specifically in how activity of one neuron is modulated by neighboring neurons. The canonical neural computation that implements such contextual influence is called divisive (or suppressive) normalization. The account proposes that this normalization is reduced in ASD. We tested one fundamental prediction of this model for low-level perception, namely that individuals with ASD would show reduced cross-orientation suppression (leading to an illusory tilt perception). 11 young adults with an ASD diagnosis and 12 age-, gender-, and IQ-matched control participants performed a psychophysical orientation perception task with compound grating stimuli. Illusory tilt perception did not differ significantly between groups, indicating typical divisive normalization in individuals with ASD. In fact, all individuals with ASD showed a considerable orientation bias. There was also no correlation between illusory tilt perception and autistic traits as measured by the Social Responsiveness Scale. These results provide clear evidence against the decreased divisive normalization model of ASD in low-level perception, where divisive normalization is best characterized. We evaluate the broader existing evidence for this model and propose ways to salvage and refine the model.

Development of Cross-Orientation Suppression and Size Tuning and the Role of Experience.

Many sensory neural circuits exhibit response normalization, which occurs when the response of a neuron to a combination of multiple stimuli is less than the sum of the responses to the individual stimuli presented alone. In the visual cortex, normalization takes the forms of cross-orientation suppression and surround suppression. At the onset of visual experience, visual circuits are partially developed and exhibit some mature features such as orientation selectivity, but it is unknown whether cross-orientation suppression is present at the onset of visual experience or requires visual experience for its emergence. We characterized the development of normalization and its dependence on visual experience in female ferrets. Visual experience was varied across the following three conditions: typical rearing, dark rearing, and dark rearing with daily exposure to simple sinusoidal gratings (14-16 h total). Cross-orientation suppression and surround suppression were noted in the earliest observations, and did not vary considerably with experience. We also observed evidence of continued maturation of receptive field properties in the second month of visual experience: substantial length summation was observed only in the oldest animals (postnatal day 90); evoked firing rates were greatly increased in older animals; and direction selectivity required experience, but declined slightly in older animals. These results constrain the space of possible circuit implementations of these features.SIGNIFICANCE STATEMENT The development of the brain depends on both nature-factors that are independent of the experience of an individual animal-and nurture-factors that depend on experience. While orientation selectivity, one of the major response properties of neurons in visual cortex, is already present at the onset of visual experience, it is unknown whether response properties that depend on interactions among multiple stimuli develop without experience. We find that the properties of cross-orientation suppression and surround suppression are present at eye opening, and do not depend on visual experience. Our results are consistent with the idea that a majority of the basic properties of sensory neurons in primary visual cortex are derived independent of the experience of an individual animal.

Measuring nonlinear signal combination using EEG.

Relatively little is known about the processes, both linear and nonlinear, by which signals are combined beyond V1. By presenting two stimulus components simultaneously, flickering at different temporal frequencies (frequency tagging) while measuring steady-state visual evoked potentials, we can assess responses to the individual components, including direct measurements of suppression on each other, and various nonlinear responses to their combination found at intermodulation frequencies. The result is a rather rich dataset of frequencies at which responses can be found. We presented pairs of sinusoidal gratings at different temporal frequencies, forming plaid patterns that were "coherent" (looking like a checkerboard) and "noncoherent" (looking like a pair of transparently overlaid gratings), and found clear intermodulation responses to compound stimuli, indicating nonlinear summation. This might have been attributed to cross-orientation suppression except that the pattern of intermodulation responses differed for coherent and noncoherent patterns, whereas the effects of suppression (measured at the component frequencies) did not. A two-stage model of nonlinear summation involving conjunction detection with a logical AND gate described the data well, capturing the difference between coherent and noncoherent plaids over a wide array of possible response frequencies. Multistimulus frequency-tagged EEG in combination with computational modeling may be a very valuable tool in studying the conjunction of these signals. In the current study the results suggest a second-order mechanism responding selectively to coherent plaid patterns.

Cross-orientation suppression in visual area V2

Object recognition relies on a series of transformations among which only the first cortical stage is relatively well understood. Already at the second stage, the visual area V2, the complexity of the transformation precludes a clear understanding of what specifically this area computes. Previous work has found multiple types of V2 neurons, with neurons of each type selective for multi-edge features. Here we analyse responses of V2 neurons to natural stimuli and find three organizing principles. First, the relevant edges for V2 neurons can be grouped into quadrature pairs, indicating invariance to local translation. Second, the excitatory edges have nearby suppressive edges with orthogonal orientations. Third, the resulting multi-edge patterns are repeated in space to form textures or texture boundaries. The cross-orientation suppression increases the sparseness of responses to natural images based on these complex forms of feature selectivity while allowing for multiple scales of position invariance.

Functional implications of orientation maps in primary visual cortex.

Stimulus orientation in the primary visual cortex of primates and carnivores is mapped as iso-orientation domains radiating from pinwheel centres, where orientation preferences of neighbouring cells change circularly. Whether this orientation map has a function is currently debated, because many mammals, such as rodents, do not have such maps. Here we show that two fundamental properties of visual cortical responses, contrast saturation and cross-orientation suppression, are stronger within cat iso-orientation domains than at pinwheel centres. These differences develop when excitation (not normalization) from neighbouring oriented neurons is applied to different cortical orientation domains and then balanced by inhibition from un-oriented neurons. The functions of the pinwheel mosaic emerge from these local intra-cortical computations: Narrower tuning, greater cross-orientation suppression and higher contrast gain of iso-orientation cells facilitate extraction of object contours from images, whereas broader tuning, greater linearity and less suppression of pinwheel cells generate selectivity for surface patterns and textures.

The Whole is Other Than the Sum: Perceived Contrast Summation Within Color and Luminance Plaids.

The apparent contrast of a plaid is a reflection of the neural relationship between the responses to its two orthogonal component gratings. To investigate the perceived contrast summation of the responses to component gratings in plaids, we compared the apparent contrasts of monocular plaids to a component grating presented alone across chromaticity and spatial frequency. Observers performed a contrast-matching task for red–green color and luminance stimuli at low- and medium-spatial frequencies. Using the measured points of subjective equality between plaids and gratings, we evaluate perceived contrast summation across conditions, which may vary between 1 (no summation) and 2 (full summation). We show that achromatic plaids have higher perceived contrast summation than chromatic plaids. The greatest difference occurs at the medium-spatial frequency, with summation highest for achromatic plaids (1.87) and lowest for chromatic plaids (1.49), while at low-spatial frequencies, there is a smaller summation difference between achromatic (1.72) and chromatic (1.65) plaids. These results are consistent with recent theories of distinct cross-orientation suppression and summation mechanisms in color and luminance vision. Two control experiments for binocular versus monocular viewing, and the overall size of the stimulus patches did not reveal any differences from our main results.

Conjectures regarding the nonlinear geometry of visual neurons

From the earliest stages of sensory processing, neurons show inherent non-linearities: the response to a complex stimulus is not a sum of the responses to a set of constituent basis stimuli. These non-linearities come in a number of forms and have been explained in terms of a number of functional goals. The family of spatial non-linearities have included interactions that occur both within and outside of the classical receptive field. They include, saturation, cross orientation inhibition, contrast normalization, end-stopping and a variety of non-classical effects. In addition, neurons show a number of facilitatory and invariance related effects such as those exhibited by complex cells (integration across position). Here, we describe an approach that attempts to explain many of the non-linearities under a single geometric framework. In line with Zetzsche and colleagues (e.g., Zetzsche et al., 1999) we propose that many of the principal non-linearities can be described by a geometry where the neural response space has a simple curvature. In this paper, we focus on the geometry that produces both increased selectivity (curving outward) and increased tolerance (curving inward). We demonstrate that overcomplete sparse coding with both low-dimensional synthetic data and high-dimensional natural scene data can result in curvature that is responsible for a variety of different known non-classical effects including end-stopping and gain control. We believe that this approach provides a more fundamental explanation of these non-linearities and does not require that one postulate a variety of explanations (e.g., that gain must be controlled or the ends of lines must be detected). In its standard form, sparse coding does not however, produce invariance/tolerance represented by inward curvature. We speculate on some of the requirements needed to produce such curvature.

The responses of V1 cortical neurons to flashed presentations of orthogonal single lines and edges.

How cortical neurons process multiple inputs is a fundamental issue in modern neuroscience. Neurons in visual cortical area V1 have been shown to exhibit cross-orientation suppression, where the response to an optimally oriented visual stimulus is reduced by the simultaneous presence of an orthogonally oriented stimulus. This is consistent with the view that cortical neurons respond to multiple inputs with a weighted average (or normalization) of the responses to the inputs presented separately. However, most of these studies have used drifting or counterphase-modulated grating stimuli, potentially confounding orientation effects with non-orientation-specific gain control mechanisms. Additionally, primate vision depends to a great extent on transient stimulus presentations during fixations between saccades. Therefore this study examined the responses of primate V1 neurons to orthogonal flashed-onset single edges and lines, and to their combinations. Single edges or lines do not typically cause strong suppression of the responses to an orthogonal stimulus, even though a grating does. This appears to hold true regardless of the relative contrasts of the orthogonal single lines or edges. This is consistent with response suppression from an orthogonal grating being due to non-orientation-specific contrast gain control (Koeling M, Shapley R, Shelley M. J Comp Neurosci 25: 390-400, 2008; Priebe NJ, Ferster D. Nat Neurosci 9: 552-561, 2006; Walker GA, Ohzawa I, Freeman RD. J.Neurophysiol 79: 227-239, 1998). While normalization mechanisms are clearly important for the cerebral cortex, under many conditions the responses of V1 cortical neurons to an optimally oriented stimulus can be unaffected by the presence of orthogonal stimuli, which may be important to avoid confounding the interpretation of a neural response.

Spatiotemporal Dynamics of Neural Fields on Product Spaces

Motivated by the functional architecture of the primary visual cortex, we analyze solutions to a neural field equation defined on the product space $\mathbb{R}\times S^1$, where the circle $S^1$ represents the orientation preferences of neurons. We show how standard solutions such as orientation bumps in $S^1$ and traveling wavefronts in $\mathbb{R}$ can destabilize in the presence of this product structure. Using bifurcation theory, we derive amplitude equations describing the spatiotemporal evolution of these instabilities. In the case of destabilization of an orientation bump, we find that synaptic weight kernels representing the patchiness of horizontal cortical connections yield new stable pattern forming solutions. For traveling wavefronts, we find that cross-orientation inhibition induces the formation of a stable propagating orientation bump at the location of the wavefront.

Visual Nonclassical Receptive Field Effects Emerge from Sparse Coding in a Dynamical System

Extensive electrophysiology studies have shown that many V1 simple cells have nonlinear response properties to stimuli within their classical receptive field (CRF) and receive contextual influence from stimuli outside the CRF modulating the cell's response. Models seeking to explain these non-classical receptive field (nCRF) effects in terms of circuit mechanisms, input-output descriptions, or individual visual tasks provide limited insight into the functional significance of these response properties, because they do not connect the full range of nCRF effects to optimal sensory coding strategies. The (population) sparse coding hypothesis conjectures an optimal sensory coding approach where a neural population uses as few active units as possible to represent a stimulus. We demonstrate that a wide variety of nCRF effects are emergent properties of a single sparse coding model implemented in a neurally plausible network structure (requiring no parameter tuning to produce different effects). Specifically, we replicate a wide variety of nCRF electrophysiology experiments (e.g., end-stopping, surround suppression, contrast invariance of orientation tuning, cross-orientation suppression, etc.) on a dynamical system implementing sparse coding, showing that this model produces individual units that reproduce the canonical nCRF effects. Furthermore, when the population diversity of an nCRF effect has also been reported in the literature, we show that this model produces many of the same population characteristics. These results show that the sparse coding hypothesis, when coupled with a biophysically plausible implementation, can provide a unified high-level functional interpretation to many response properties that have generally been viewed through distinct mechanistic or phenomenological models.

A model of binocular rivalry and cross-orientation suppression.

Binocular rivalry and cross-orientation suppression are well-studied forms of competition in visual cortex, but models of these two types of competition are in tension with one another. Binocular rivalry occurs during the presentation of dichoptic grating stimuli, where two orthogonal gratings presented separately to the two eyes evoke strong alternations in perceptual dominance. Cross-orientation suppression occurs during the presentation of plaid stimuli, where the responses to a component grating presented to both eyes is weakened by the presence of a superimposed orthogonal grating. Conventional models of rivalry that rely on strong competition between orientation-selective neurons incorrectly predict rivalry between the components of plaids. Lowering the inhibitory weights in such models reduces rivalry for plaids, but also reduces it for dichoptic gratings. Using an exhaustive grid search, we show that this problem cannot be solved simply by adjusting the parameters of the model. Instead, we propose a robust class of models that rely on ocular opponency neurons, previously proposed as a mechanism for efficient stereo coding, to yield rivalry only for dichoptic gratings, not for plaids. This class of models reconciles models of binocular rivalry with the divisive normalization framework that has been used to explain cross-orientation. Our model makes novel predictions that we confirmed with psychophysical tests.

Temporal Evolution of Pattern Disparity Processing in Humans

Stereo matching, i.e., the matching by the visual system of corresponding parts of the images seen by the two eyes, is inherently a 2D problem. To gain insights into how this operation is carried out by the visual system, we measured, in human subjects, the reflexive vergence eye movements elicited by the sudden presentation of stereo plaids. We found compelling evidence that the 2D pattern disparity is computed by combining disparities first extracted within orientation selective channels. This neural computation takes 10-15 ms, and is carried out even when subjects perceive not a single plaid but rather two gratings in different depth planes (transparency). However, we found that 1D disparities are not always effectively combined: when spatial frequency and contrast of the gratings are sufficiently different pattern disparity is not computed, a result that cannot be simply attributed to the transparency of such stimuli. Based on our results, we propose that a narrow-band implementation of the IOC (Intersection of Constraints) rule (Fennema and Thompson, 1979; Adelson and Movshon, 1982), preceded by cross-orientation suppression, underlies the extraction of pattern disparity.

Effects of texture component orientation on orientation flow visibility for 3-D shape perception.

In images of textured 3-D surfaces, orientation flows created by the texture components parallel to the surface slant play a critical role in conveying the surface slant and shape. This study examines the visibility of these orientation flows in complex patterns. Specifically, we examine the effect of orientation of neighboring texture components on orientation flow visibility. Complex plaids consisting of gratings equally spaced in orientation were mapped onto planar and curved surfaces. The visibility of the component that creates the orientation flows was quantified by measuring its contrast threshold (CT) while varying the combination of neighboring components present in the pattern. CTs were consistently lowest only when components closest in orientation to that of the orientation flows were subtracted from the pattern. This finding suggests that a previously reported frequency-selective cross-orientation suppression mechanism involved with the perception of 3-D shape from texture is affected by proximity in orientation of concurrent texture components.