Size tuning of neural response variability in laminar circuits of macaque primary visual cortex.

A defining feature of the cortex is its laminar organization, which is likely critical for cortical information processing. For example, visual stimuli of different size evoke distinct patterns of laminar activity. Visual information processing is also influenced by the response variability of individual neurons and the degree to which this variability is correlated among neurons. To elucidate laminar processing, we studied how neural response variability across the layers of macaque primary visual cortex is modulated by visual stimulus size. Our laminar recordings revealed that single neuron response variability and the shared variability among neurons are tuned for stimulus size, and this size-tuning is layer-dependent. In all layers, stimulation of the receptive field (RF) reduced single neuron variability, and the shared variability among neurons, relative to their pre-stimulus values. As the stimulus was enlarged beyond the RF, both single neuron and shared variability increased in supragranular layers, but either did not change or decreased in other layers. Surprisingly, we also found that small visual stimuli could increase variability relative to baseline values. Our results suggest multiple circuits and mechanisms as the source of variability in different layers and call for the development of new models of neural response variability.

Distinct Laminar Processing of Local and Global Context in Primate Primary Visual Cortex.

Visual perception is affected by spatial context. In visual cortex, neuronal responses to stimuli inside the receptive field (RF) are suppressed by stimuli in the RF surround. To understand the circuits and cortical layers processing spatial context, we simultaneously recorded across all layers of macaque primary visual cortex while presenting stimuli at increasing distances from the recorded cells' RF. We find that near versus far-surround stimuli activate distinct layers, thus revealing unique laminar contributions to the processing of local and global spatial context. Stimuli in the near-surround evoke the earliest subthreshold responses in superficial and upper-deep layers, and earliest suppression of spiking responses in superficial layers. Conversely, far-surround stimuli evoke the earliest subthreshold responses in feedback-recipient layer 1 and lower-deep layers, and earliest suppression of spiking responses almost simultaneously in all layers, except 4C, where suppression emerges last. Our results suggest distinct circuits for local and global signal integration.

Top-down feedback controls spatial summation and response amplitude in primate visual cortex.

Sensory information travels along feedforward connections through a hierarchy of cortical areas, which, in turn, send feedback connections to lower-order areas. Feedback has been implicated in attention, expectation, and sensory context, but the mechanisms underlying these diverse feedback functions are unknown. Using specific optogenetic inactivation of feedback connections from the secondary visual area (V2), we show how feedback affects neural responses in the primate primary visual cortex (V1). Reducing feedback activity increases V1 cells' receptive field (RF) size, decreases their responses to stimuli confined to the RF, and increases their responses to stimuli extending into the proximal surround, therefore reducing surround suppression. Moreover, stronger reduction of V2 feedback activity leads to progressive increase in RF size and decrease in response amplitude, an effect predicted by a recurrent network model. Our results indicate that feedback modulates RF size, surround suppression and response amplitude, similar to the modulatory effects of visual spatial attention.

Circuits and Mechanisms for Surround Modulation in Visual Cortex.

Surround modulation (SM) is a fundamental property of sensory neurons in many species and sensory modalities. SM is the ability of stimuli in the surround of a neuron's receptive field (RF) to modulate (typically suppress) the neuron's response to stimuli simultaneously presented inside the RF, a property thought to underlie optimal coding of sensory information and important perceptual functions. Understanding the circuit and mechanisms for SM can reveal fundamental principles of computations in sensory cortices, from mouse to human. Current debate is centered over whether feedforward or intracortical circuits generate SM, and whether this results from increased inhibition or reduced excitation. Here we present a working hypothesis, based on theoretical and experimental evidence, that SM results from feedforward, horizontal, and feedback interactions with local recurrent connections, via synaptic mechanisms involving both increased inhibition and reduced recurrent excitation. In particular, strong and balanced recurrent excitatory and inhibitory circuits play a crucial role in the computation of SM.

Multiple components of surround modulation in primary visual cortex: multiple neural circuits with multiple functions?

The responses of neurons in primary visual cortex (V1) to stimulation of their receptive field (RF) are modulated by stimuli in the RF surround. This modulation is suppressive when the stimuli in the RF and surround are of similar orientation, but less suppressive or facilitatory when they are cross-oriented. Similarly, in human vision surround stimuli selectively suppress the perceived contrast of a central stimulus. Although the properties of surround modulation have been thoroughly characterized in many species, cortical areas and sensory modalities, its role in perception remains unknown. Here we argue that surround modulation in V1 consists of multiple components having different spatio-temporal and tuning properties, generated by different neural circuits and serving different visual functions. One component arises from LGN afferents, is fast, untuned for orientation, and spatially restricted to the surround region nearest to the RF (the near-surround); its function is to normalize V1 cell responses to local contrast. Intra-V1 horizontal connections contribute a slower, narrowly orientation-tuned component to near-surround modulation, whose function is to increase the coding efficiency of natural images in manner that leads to the extraction of object boundaries. The third component is generated by topdown feedback connections to V1, is fast, broadly orientation-tuned, and extends into the far-surround; its function is to enhance the salience of behaviorally relevant visual features. Far- and near-surround modulation, thus, act as parallel mechanisms: the former quickly detects and guides saccades/attention to salient visual scene locations, the latter segments object boundaries in the scene.

Visual interactions conform to pattern decorrelation in multiple cortical areas.

Neural responses to visual stimuli are strongest in the classical receptive field, but they are also modulated by stimuli in a much wider region. In the primary visual cortex, physiological data and models suggest that such contextual modulation is mediated by recurrent interactions between cortical areas. Outside the primary visual cortex, imaging data has shown qualitatively similar interactions. However, whether the mechanisms underlying these effects are similar in different areas has remained unclear. Here, we found that the blood oxygenation level dependent (BOLD) signal spreads over considerable cortical distances in the primary visual cortex, further than the classical receptive field. This indicates that the synaptic activity induced by a given stimulus occurs in a surprisingly extensive network. Correspondingly, we found suppressive and facilitative interactions far from the maximum retinotopic response. Next, we characterized the relationship between contextual modulation and correlation between two spatial activation patterns. Regardless of the functional area or retinotopic eccentricity, higher correlation between the center and surround response patterns was associated with stronger suppressive interaction. In individual voxels, suppressive interaction was predominant when the center and surround stimuli produced BOLD signals with the same sign. Facilitative interaction dominated in the voxels with opposite BOLD signal signs. Our data was in unison with recently published cortical decorrelation model, and was validated against alternative models, separately in different eccentricities and functional areas. Our study provides evidence that spatial interactions among neural populations involve decorrelation of macroscopic neural activation patterns, and suggests that the basic design of the cerebral cortex houses a robust decorrelation mechanism for afferent synaptic input.

Fovea-periphery axis symmetry of surround modulation in the human visual system.

A visual stimulus activates different sized cortical area depending on eccentricity of the stimulus. Here, our aim is to understand whether the visual field size of a stimulus or cortical size of the corresponding representation determines how strongly it interacts with other stimuli. We measured surround modulation of blood-oxygenation-level-dependent signal and perceived contrast with surrounds that extended either towards the periphery or the fovea from a center stimulus, centered at 6° eccentricity. This design compares the effects of two surrounds which are identical in visual field size, but differ in the sizes of their cortical representations. The surrounds produced equally strong suppression, which suggests that visual field size of the surround determines suppression strength. A modeled population of neuronal responses, in which all the parameters were experimentally fixed, captured the pattern of results both in psychophysics and functional magnetic resonance imaging. Although the fovea-periphery anisotropy affects nearly all aspects of spatial vision, our results suggest that in surround modulation the visual system compensates for it.

Different orientation tuning of near- and far-surround suppression in macaque primary visual cortex mirrors their tuning in human perception.

In primary visual cortex (V1), neuronal responses to stimuli inside the receptive field (RF) are usually suppressed by stimuli in the RF surround. This suppression is orientation specific. Similarly, in human vision surround stimuli can suppress perceived contrast of a central stimulus in an orientation-dependent manner. The surround consists of two regions likely generated by different circuits: a near-surround generated predominantly by geniculocortical and intra-V1 horizontal connections, and a far-surround generated exclusively by interareal feedback. Using stimuli confined to the near- or far-surround of V1 neurons, and similar stimuli in human psychophysics, we find that near-surround suppression is more sharply orientation tuned than far-surround suppression in both macaque V1 and human perception. These results point to a similarity between surround suppression in macaque V1 and human vision, and suggest that feedback circuits are less orientation biased than horizontal circuits. We find the sharpest tuning of near-surround suppression in V1 layers (3, 4B, 4Cα) with patterned and orientation-specific horizontal connections. Sharpest tuning of far-surround suppression occurs in layer 4B, suggesting greater orientation specificity of feedback to this layer. Different orientation tuning of near- and far-surround suppression may reflect a statistical bias in natural images, whereby nearby edges have higher probability than distant edges of being co-oriented and belonging to the same contour. Surround suppression would, thus, increase the coding efficiency of frequently co-occurring contours and the saliency of less frequent ones. Such saliency increase can help detect small orientation differences in nearby edges (for contour completion), but large orientation differences in distant edges (for directing saccades/attention).

The effect of mean luminance change and grating pedestals on contrast perception: model simulations suggest a common, retinal, origin.

The percept of a contrast target is substantially affected by co-occurring changes in mean luminance or underlying ("pedestal") contrast elements. These two types of modulatory effects have traditionally been studied as separate phenomena. However, regardless of different higher-level mechanisms, both classes of phenomena will necessarily also depend on shared mechanisms in the first stages of vision, starting with the primary responses of photoreceptors. Here we present model simulations showing that important aspects of both classes may be explained by the temporal dynamics of photoreceptor responses read by integrate-and-fire operators. The model is physiologically justified and all its parameters are constrained by experimental evidence. Although there remains plenty of room for additional mechanisms to shape the exact quantitative realization of the perceptual functions in different situations, we suggest that signature features may be inherited from primary retinal signaling.

Effects of mean luminance changes on human contrast perception: contrast dependence, time-course and spatial specificity.

BACKGROUND: When we are viewing natural scenes, every saccade abruptly changes both the mean luminance and the contrast structure falling on any given retinal location. Thus it would be useful if the two were independently encoded by the visual system, even when they change simultaneously. Recordings from single neurons in the cat visual system have suggested that contrast information may be quite independently represented in neural responses to simultaneous changes in contrast and luminance. Here we test to what extent this is true in human perception. METHODOLOGY/PRINCIPAL FINDINGS: Small contrast stimuli were presented together with a 7-fold upward or downward step of mean luminance (between 185 and 1295 Td, corresponding to 14 and 98 cd/m(2)), either simultaneously or with various delays (50-800 ms). The perceived contrast of the target under the different conditions was measured with an adaptive staircase method. Over the contrast range 0.1-0.45, mainly subtractive attenuation was found. Perceived contrast decreased by 0.052±0.021 (N = 3) when target onset was simultaneous with the luminance increase. The attenuation subsided within 400 ms, and even faster after luminance decreases, where the effect was also smaller. The main results were robust against differences in target types and the size of the field over which luminance changed. CONCLUSIONS/SIGNIFICANCE: Perceived contrast is attenuated mainly by a subtractive term when coincident with a luminance change. The effect is of ecologically relevant magnitude and duration; in other words, strict contrast constancy must often fail during normal human visual behaviour. Still, the relative robustness of the contrast signal is remarkable in view of the limited dynamic response range of retinal cones. We propose a conceptual model for how early retinal signalling may allow this.

Surround suppression and facilitation in the fovea: very long-range spatial interactions in contrast perception.

Surround modulation of perceived contrast has been almost exclusively studied in short-range conditions, i.e., in situations where a tiny gap, at most, separates center from surround. Existing long-range studies suggest that suppression extends to 12-cycle distance, whereas facilitation of perceived contrast is suggested to arise from visual field regions enclosing the center. In V1 neurons, however, long-range surround modulation involves both suppression and facilitation. Thus, we investigated short- and long-range surround modulation by measuring the perceived contrast of a center in the presence of a surround either near (0.3 cycles, 0.1 degree) or far (19.8 cycles, 6.6 degrees) from the center. This study demonstrates that in addition to the well-known suppression, surround modulation involves remarkably long-range facilitation of perceived contrast. At low center contrasts, the long-range facilitation was stronger than the long-range suppression, whereas at high center contrast we found mainly long-range suppression. Because the current models of perceived contrast could not account for our data, we considered our results in the context of models developed for surround modulation in V1 neurons. However, neither mechanistic nor phenomenological models proved satisfactory. Moreover, with the current knowledge, it seems that straightforward pooling of V1 neurons' responses cannot account for surround modulation of perceived contrast.

Area summation in human visual system: psychophysics, fMRI, and modeling.

Contextual modulation is a fundamental feature of sensory processing, both on perceptual and on single-neuron level. When the diameter of a visual stimulus is increased, the firing rate of a cell typically first increases (summation field) and then decreases (surround field). Such an area summation function draws a comprehensive profile of the receptive field structure of a neuron, including areas outside the classical receptive field. We investigated area summation in human vision with psychophysics and functional magnetic resonance imaging (fMRI). The stimuli were drifting sine wave gratings similar to those used in previous macaque single-cell area summation studies [corrected]. A model was developed to facilitate comparison of area summation in fMRI to area summation in psychophysics and single cells. The model consisted of units with an antagonistic receptive field structure found in single cells in the primary visual cortex. The receptive field centers of the model neurons were distributed in the region of the visual field covered by a single voxel. The measured area summation functions were qualitatively similar to earlier single-cell data. The model with parameters derived from psychophysics captured the spatial structure of the summation field in the primary visual cortex as measured with fMRI. The model also generalized to a novel situation in which the neural population was displaced from the stimulus center. The current study shows that contextual modulation arises from similar spatially antagonistic and overlapping excitatory and inhibitory mechanisms, both in single cells and in human vision.

Spatial frequency tuning in human retinotopic visual areas.

Human medial occipital cortex comprises multiple visual areas, each with a distinct retinotopic representation of visual environment. We measured spatial frequency (SF) tuning curves with functional magnetic resonance imaging (fMRI) and found consistent differences between these areas. Areas V1, V2, VP, V3, V4v, and V3A were all band-pass tuned, with progressively lower SF optima in V1, V2, and V3A. In VP and V3, the SF optima were similar to optima in V2, whereas V4v showed more individual variation and scattered SF representations on the cortical surface. Area V5+ showed low-pass SF tuning. In each area, the SF optimum declined with increasing eccentricity. After accounting for the cortical magnification, the cortical extent of the optimal spatial wavelengths was approximately constant across eccentricity in V1, which suggests an anatomical constraint for the optimal SF, and this extent is actually comparable to the extent of horizontal connections within primate V1. The optimal spatial wavelengths in the visual field are also of similar extent to the spatial summation fields of macaque V1. The progressive decline in the SF tuning from V1 to V2 and V3A is compatible with the view that these areas represent visual information at different spatial scales.