Neural Correlates of Crowding in Macaque Area V4.

Visual crowding refers to the phenomenon where a target object that is easily identifiable in isolation becomes difficult to recognize when surrounded by other stimuli (distractors). Many psychophysical studies have investigated this phenomenon and proposed alternative models for the underlying mechanisms. One prominent hypothesis, albeit with mixed psychophysical support, posits that crowding arises from the loss of information due to pooled encoding of features from target and distractor stimuli in the early stages of cortical visual processing. However, neurophysiological studies have not rigorously tested this hypothesis. We studied the responses of single neurons in macaque (one male, one female) area V4, an intermediate stage of the object-processing pathway, to parametrically designed crowded displays and texture statistics-matched metameric counterparts. Our investigations reveal striking parallels between how crowding parameters-number, distance, and position of distractors-influence human psychophysical performance and V4 shape selectivity. Importantly, we also found that enhancing the salience of a target stimulus could alleviate crowding effects in highly cluttered scenes, and this could be temporally protracted reflecting a dynamical process. Thus, a pooled encoding of nearby stimuli cannot explain the observed responses, and we propose an alternative model where V4 neurons preferentially encode salient stimuli in crowded displays. Overall, we conclude that the magnitude of crowding effects is determined not just by the number of distractors and target-distractor separation but also by the relative salience of targets versus distractors based on their feature attributes-the similarity of distractors and the contrast between target and distractor stimuli.

Perceptual Texture Dimensions Modulate Neuronal Response Dynamics in Visual Cortical Area V4.

Texture is an important visual attribute for surface pattern discrimination and therefore object segmentation, but the neural bases of texture perception are largely unknown. Previously, we demonstrated that the responses of V4 neurons to naturalistic texture patches are sensitive to four key features of human texture perception: coarseness, directionality, regularity, and contrast. To begin to understand how distinct texture perception emerges from the dynamics of neuronal responses, in 2 macaque monkeys (1 male, 1 female), we investigated the relative contribution of the four texture attributes to V4 responses in terms of the strength and timing of response modulation. We found that the different feature dimensions are associated with different temporal dynamics. Specifically, the response modulation associated with directionality and regularity was significantly delayed relative to that associated with coarseness and contrast, suggesting that the latter are fundamentally simpler feature dimensions. The population of texture-selective neurons could be grouped into multiple clusters based on the combination of feature dimensions encoded, and those subpopulations displayed distinct temporal dynamics characterized by the weighted combinations of multiple features. Finally, we applied a population decoding approach to demonstrate that texture category information can be obtained from short temporal windows across time. These results demonstrate that the representation of different perceptually relevant texture features emerge over time in the responses of V4 neurons. The observed temporal organization provides a framework to interpret how the processing of surface features unfolds in early and midlevel cortical stages, and could ultimately inform the interpretation of perceptual texture dynamics.SIGNIFICANCE STATEMENT To delineate how neuronal responses underlie our ability to perceive visual textures, we related four key perceptual dimensions (coarseness, directionality, regularity, and contrast) of naturalistic textures to the strength and timing of modulation of neuronal responses in area V4, an intermediate stage in the form-processing, ventral visual pathway. Our results provide the first characterization of V4 temporal dynamics for texture encoding along perceptually defined axes.

Neural Coding for Shape and Texture in Macaque Area V4.

The distinct visual sensations of shape and texture have been studied separately in cortex; therefore, it remains unknown whether separate neuronal populations encode each of these properties or one population carries a joint encoding. We directly compared shape and texture selectivity of individual V4 neurons in awake macaques (1 male, 1 female) and found that V4 neurons lie along a continuum from strong tuning for boundary curvature of shapes to strong tuning for perceptual dimensions of texture. Among neurons tuned to both attributes, tuning for shape and texture were largely separable, with the latter delayed by ∼30 ms. We also found that shape stimuli typically evoked stronger, more selective responses than did texture patches, regardless of whether the latter were contained within or extended beyond the receptive field. These results suggest that there are separate specializations in mid-level cortical processing for visual attributes of shape and texture.SIGNIFICANCE STATEMENT Object recognition depends on our ability to see both the shape of the boundaries of objects and properties of their surfaces. However, neuroscientists have never before examined how shape and texture are linked together in mid-level visual cortex. In this study, we used systematically designed sets of simple shapes and texture patches to probe the responses of individual neurons in the primate visual cortex. Our results provide the first evidence that some cortical neurons specialize in processing shape whereas others specialize in processing textures. Most neurons lie between the ends of this continuum, and in these neurons we find that shape and texture encoding are largely independent.

Binocular function during unequal monocular input.

The fine task of stereoscopic depth discrimination in human subjects requires a functional binocular system. Behavioral investigations show that relatively small binocular abnormalities can diminish stereoscopic acuity. Clinical evaluations are consistent with this observation. Neurons in visual cortex represent the first stage of processing of the binocular system. Cells at this level are generally acutely sensitive to differences in relative depth. However, an apparent paradox in previous work demonstrates that tuning for binocular disparities remains relatively constant even when large contrast differences are imposed between left and right eye stimuli. This implies a range of neural binocular function that is at odds with behavioral findings. To explore this inconsistency, we have conducted psychophysical tests by which human subjects view vertical sinusoidal gratings drifting in opposite directions to left and right eyes. If the opposite drifting gratings are integrated in visual cortex, as wave theory and neurophysiological data predict, the subjects should perceive a fused stationary grating that is counter-phasing in place. However, this behavioral combination may not occur if there are differences in contrast and therefore signal strength between left and right eye stimuli. As expected for the control condition, our results show fused counter-phase perception for equal inter-ocular grating contrasts. Our experimental tests show a striking retention of counter-phase perception even for relatively large differences in inter-ocular contrast. This finding demonstrates that binocular integration, although relatively coarse, can occur during substantial differences in left and right eye signal strength.

Direction selectivity of neurons in the visual cortex is non-linear and lamina-dependent.

Neurons in the visual cortex are generally selective to direction of movement of a stimulus. Although models of this direction selectivity (DS) assume linearity, experimental data show stronger degrees of DS than those predicted by linear models. Our current study was intended to determine the degree of non-linearity of the DS mechanism for cells within different laminae of the cat's primary visual cortex. To do this, we analysed cells in our database by using neurophysiological and histological approaches to quantify non-linear components of DS in four principal cortical laminae (layers 2/3, 4, 5, and 6). We used a DS index (DSI) to quantify degrees of DS in our sample. Our results showed laminar differences. In layer 4, the main thalamic input region, most neurons were of the simple type and showed high DSI values. For complex cells in layer 4, there was a broad distribution of DSI values. Similar features were observed in layer 2/3, but complex cells were dominant. In deeper layers (5 and 6), DSI value distributions were characterized by clear peaks at high values. Independently of specific lamina, high DSI values were accompanied by narrow orientation tuning widths. Differences in orientation tuning for non-preferred vs. preferred directions were smallest in layer 4 and largest in layer 6. These results are consistent with a non-linear process of intra-cortical inhibition that enhances DS by selective suppression of neuronal firing for non-preferred directions of stimulus motion in a lamina-dependent manner. Other potential mechanisms are also considered.

Neural correlates of crowding in macaque area V4.

Visual crowding refers to the phenomenon where a target object that is easily identifiable in isolation becomes difficult to recognize when surrounded by other stimuli (distractors). Extensive psychophysical studies support two alternative possibilities for the underlying mechanisms. One hypothesis suggests that crowding results from the loss of visual information due to pooled encoding of multiple nearby stimuli in the mid-level processing stages along the ventral visual pathway. Alternatively, crowding may arise from limited resolution in decoding object information during recognition and the encoded information may remain inaccessible unless it is salient. To rigorously test these alternatives, we studied the responses of single neurons in macaque area V4, an intermediate stage of the ventral, object-processing pathway, to parametrically designed crowded displays and their texture-statistics matched metameric counterparts. Our investigations reveal striking parallels between how crowding parameters, e.g., number, distance, and position of distractors, influence human psychophysical performance and V4 shape selectivity. Importantly, we found that enhancing the salience of a target stimulus could reverse crowding effects even in highly cluttered scenes and such reversals could be protracted reflecting a dynamical process. Overall, we conclude that a pooled encoding of nearby stimuli cannot explain the observed responses and we propose an alternative model where V4 neurons preferentially encode salient stimuli in crowded displays.

Dissociation in neuronal encoding of object versus surface motion in the primate brain.

A paradox exists in our understanding of motion processing in the primate visual system: neurons in the dorsal motion processing stream often strikingly fail to encode long-range and perceptually salient jumps of a moving stimulus. Psychophysical studies suggest that such long-range motion, which requires integration over more distant parts of the visual field, may be based on higher-order motion processing mechanisms that rely on feature or object tracking. Here, we demonstrate that ventral visual area V4, long recognized as critical for processing static scenes, includes neurons that maintain direction selectivity for long-range motion, even when conflicting local motion is present. These V4 neurons exhibit specific selectivity for the motion of objects, i.e., targets with defined boundaries, rather than the motion of surfaces behind apertures, and are selective for direction of motion over a broad range of spatial displacements and defined by a variety of features. Motion direction at a range of speeds can be accurately decoded on single trials from the activity of just a few V4 neurons. Thus, our results identify a novel motion computation in the ventral stream that is strikingly different from, and complementary to, the well-established system in the dorsal stream, and they support the hypothesis that the ventral stream system interacts with the dorsal stream to achieve the higher level of abstraction critical for tracking dynamic objects.

Visual Functions of Primate Area V4.

Area V4-the focus of this review-is a mid-level processing stage along the ventral visual pathway of the macaque monkey. V4 is extensively interconnected with other visual cortical areas along the ventral and dorsal visual streams, with frontal cortical areas, and with several subcortical structures. Thus, it is well poised to play a broad and integrative role in visual perception and recognition-the functional domain of the ventral pathway. Neurophysiological studies in monkeys engaged in passive fixation and behavioral tasks suggest that V4 responses are dictated by tuning in a high-dimensional stimulus space defined by form, texture, color, depth, and other attributes of visual stimuli. This high-dimensional tuning may underlie the development of object-based representations in the visual cortex that are critical for tracking, recognizing, and interacting with objects. Neurophysiological and lesion studies also suggest that V4 responses are important for guiding perceptual decisions and higher-order behavior.

Object shape and surface properties are jointly encoded in mid-level ventral visual cortex.

Recognizing a myriad visual objects rapidly is a hallmark of the primate visual system. Traditional theories of object recognition have focused on how crucial form features, for example, the orientation of edges, may be extracted in early visual cortex and utilized to recognize objects. An alternative view argues that much of early and mid-level visual processing focuses on encoding surface characteristics, for example, texture. Neurophysiological evidence from primate area V4 supports a third alternative - the joint, but independent, encoding of form and texture - that would be advantageous for segmenting objects from the background in natural scenes and for object recognition that is independent of surface texture. Future studies that leverage deep convolutional network models, especially focusing on network failures to match biology and behavior, can advance our insights into how such a joint representation of form and surface properties might emerge in visual cortex.

Covariation between Spike and LFP Modulations Revealed with Focal and Asynchronous Stimulation of Receptive Field Surround in Monkey Primary Visual Cortex.

A focal visual stimulus outside the classical receptive field (RF) of a V1 neuron does not evoke a spike response by itself, and yet evokes robust changes in the local field potential (LFP). This subthreshold LFP provides a unique opportunity to investigate how changes induced by surround stimulation leads to modulation of spike activity. In the current study, two identical Gabor stimuli were sequentially presented with a variable stimulus onset asynchrony (SOA) ranging from 0 to 100 ms: the first (S1) outside the RF and the second (S2) over the RF of primary visual cortex neurons, while trained monkeys performed a fixation task. This focal and asynchronous stimulation of the RF surround enabled us to analyze the modulation of S2-evoked spike activity and covariation between spike and LFP modulation across SOA. In this condition, the modulation of S2-evoked spike response was dominantly facilitative and was correlated with the change in LFP amplitude, which was pronounced for the cells recorded in the upper cortical layers. The time course of covariation between the SOA-dependent spike modulation and LFP amplitude suggested that the subthreshold LFP evoked by the S1 can predict the magnitude of upcoming spike modulation.

Transcranial Magnetic Stimulation Changes Response Selectivity of Neurons in the Visual Cortex.

BACKGROUND: Transcranial magnetic stimulation (TMS) is used to selectively alter neuronal activity of specific regions in the cerebral cortex. TMS is reported to induce either transient disruption or enhancement of different neural functions. However, its effects on tuning properties of sensory neurons have not been studied quantitatively. OBJECTIVE/HYPOTHESIS: Here, we use specific TMS application parameters to determine how they may alter tuning characteristics (orientation, spatial frequency, and contrast sensitivity) of single neurons in the cat's visual cortex. METHODS: Single unit spikes were recorded with tungsten microelectrodes from the visual cortex of anesthetized and paralyzed cats (12 males). Repetitive TMS (4 Hz, 4 s) was delivered with a 70 mm figure-8 coil. We quantified basic tuning parameters of individual neurons for each pre- and post-TMS condition. The statistical significance of changes for each tuning parameter between the two conditions was evaluated with a Wilcoxon signed-rank test. RESULTS: We generally find long-lasting suppression which persists well beyond the stimulation period. Pre- and post-TMS orientation tuning curves show constant peak values. However, strong suppression at non-preferred orientations tends to narrow the widths of tuning curves. Spatial frequency tuning exhibits an asymmetric change in overall shape, which results in an emphasis on higher frequencies. Contrast tuning curves show nonlinear changes consistent with a gain control mechanism. CONCLUSIONS: These findings suggest that TMS causes extended interruption of the balance between sub-cortical and intra-cortical inputs.

Modulation of V1 spike response by temporal interval of spatiotemporal stimulus sequence.

The spike activity of single neurons of the primary visual cortex (V1) becomes more selective and reliable in response to wide-field natural scenes compared to smaller stimuli confined to the classical receptive field (RF). However, it is largely unknown what aspects of natural scenes increase the selectivity of V1 neurons. One hypothesis is that modulation by surround interaction is highly sensitive to small changes in spatiotemporal aspects of RF surround. Such a fine-tuned modulation would enable single neurons to hold information about spatiotemporal sequences of oriented stimuli, which extends the role of V1 neurons as a simple spatiotemporal filter confined to the RF. In the current study, we examined the hypothesis in the V1 of awake behaving monkeys, by testing whether the spike response of single V1 neurons is modulated by temporal interval of spatiotemporal stimulus sequence encompassing inside and outside the RF. We used two identical Gabor stimuli that were sequentially presented with a variable stimulus onset asynchrony (SOA): the preceding one (S1) outside the RF and the following one (S2) in the RF. This stimulus configuration enabled us to examine the spatiotemporal selectivity of response modulation from a focal surround region. Although S1 alone did not evoke spike responses, visual response to S2 was modulated for SOA in the range of tens of milliseconds. These results suggest that V1 neurons participate in processing spatiotemporal sequences of oriented stimuli extending outside the RF.