Perceptual organization of local elements into global shapes in the human visual cortex

The question of how local image features on the retina are integrated into perceived global shapes is central to our understanding of human visual perception. Psychophysical investigations have suggested that the emergence of a coherent visual percept, or a "good-Gestalt", is mediated by the perceptual organization of local features based on their similarity. However, the neural mechanisms that mediate unified shape perception in the human brain remain largely unknown. Using human fMRI, we demonstrate that not only higher occipitotemporal but also early retinotopic areas are involved in the perceptual organization and detection of global shapes. Specifically, these areas showed stronger fMRI responses to global contours consisting of collinear elements than to patterns of randomly oriented local elements. More importantly, decreased detection performance and fMRI activations were observed when misalignment of the contour elements disturbed the perceptual coherence of the contours. However, grouping of the misaligned contour elements by disparity resulted in increased performance and fMRI activations, suggesting that similar neural mechanisms may underlie grouping of local elements to global shapes by different visual features (orientation or disparity). Thus, these findings provide novel evidence for the role of both early feature integration processes and higher stages of visual analysis in coherent visual perception.     

Remembering visual motion: neural correlates of associative plasticity and motion recall in cortical area MT

The pictorial content of visual memories recalled by association is embodied by neuronal activity at the highest processing stages of primate visual cortex. This activity is elicited by top-down signals from the frontal lobe and recapitulates the bottom-up pattern normally obtained by the recalled stimulus. To explore the generality and mechanisms of this phenomenon, we recorded motion-sensitive neurons at an early stage of cortical processing. After monkeys learned to associate directions of motion with static shapes, these neurons exhibited unprecedented selectivity for the shapes. This emergent shape selectivity reflects activation of neurons representing the motion stimuli recalled by association, and it suggests that recall-related activity may be a general feature of neurons in visual cortex.     

The inferior temporal cortex: Architecture, computation, and representation

Neurons in the inferior temporal cortex (IT), an area crucially involved in visual object recognition in monkeys, show the visual response properties and anatomical/chemical nature which are distinct from those in the cortical areas that feed visual inputs to the IT. Earlier physiological studies showed that IT neurons have large receptive fields covering the center and contralateral (often bilateral) visual fields, stimulus selectivity for images of complex objects or shapes, and translation invariance of the stimulus selectivity. Recent studies have revealed new aspects of their properties such as invariant selectivity for shapes despite drastic changes in various physical attributes of stimuli, latent excitatory inputs masked by stimulus-specific GABAergic inhibition, selectivity for binocular disparity and 3-dimensional surface structures, profound effects of learning on the stimulus selectivity, and columnar clustering of neurons with similarstimulus selectivity for shapes and other object features. Another line of research using histological techniques have revealed that pyramidal neurons in the IT are larger in the size of dendritic arbors, in the number of dendritic branches and spines, and in the size and distribution of horizontal axonal arbors than those in the earlier areas, allowing them to integrate a larger population of afferents and process more diverse inputs. The concentration of several neurochemicals including those related to synaptic transmission or plasticity changes systematically towards the IT along the occipitotemporal pathway. Many of the characteristics of IT neurons parallel or explain certain aspects of visual object perception, although the behavioral relevance has yet to be addressed experimentally.     

Motion adaptation distorts perceived visual position

After an observer adapts to a moving stimulus, texture within a stationary stimulus is perceived to drift in the opposite direction-the traditional motion aftereffect (MAE). It has recently been shown that the perceived position of objects can be markedly influenced by motion adaptation. In the present study, we examine the selectivity of positional shifts resulting from motion adaptation to stimulus attributes such as velocity, relative contrast, and relative spatial frequency. In addition, we ask whether spatial position can be modified in the absence of perceived motion. Results show that when adapting and test stimuli have collinear carrier gratings, the global position of the object shows a substantial shift in the direction of the illusory motion. When the carrier gratings of the adapting and test stimuli are orthogonal (a configuration in which no MAE is experienced), a global positional shift of similar magnitude is found. The illusory positional shift was found to be immune to changes in spatial frequency and to contrast between adapting and test stimuli-manipulations that dramatically reduce the magnitude of the traditional MAE. The lack of sensitivity for stimulus characteristics other than direction of motion suggests that a specialized population of cortical neurones, which are insensitive to changes in a number of rudimentary visual attributes, may modulate positional representation in lower cortical areas.     

Nonmonotonic noise tuning of BOLD fMRI signal to natural images in the visual cortex of the anesthetized monkey

BACKGROUND: The perceptual ability of humans and monkeys to identify objects in the presence of noise varies systematically and monotonically as a function of how much noise is introduced to the visual display. That is, it becomes more and more difficult to identify an object with increasing noise. Here we examine whether the blood oxygen level-dependent functional magnetic resonance imaging (BOLD fMRI) signal in anesthetized monkeys also shows such monotonic tuning. We employed parametric stimulus sets containing natural images and noise patterns matched for spatial frequency and intensity as well as intermediate images generated by interpolation between natural images and noise patterns. Anesthetized monkeys provide us with the unique opportunity to examine visual processing largely in the absence of top-down cognitive modulations and can thus provide an important baseline against which work with awake monkeys and humans can be compared. RESULTS: We measured BOLD activity in occipital visual cortical areas as natural images and noise patterns, as well as intermediate interpolated patterns at three interpolation levels (25%, 50%, and 75%) were presented to anesthetized monkeys in a block paradigm. We observed reliable visual activity in occipital visual areas including V1, V2, V3, V3A, and V4 as well as the fundus and anterior bank of the superior temporal sulcus (STS). Natural images consistently elicited higher BOLD levels than noise patterns. For intermediate images, however, we did not observe monotonic tuning. Instead, we observed a characteristic V-shaped noise-tuning function in primary and extrastriate visual areas. BOLD signals initially decreased as noise was added to the stimulus but then increased again as the pure noise pattern was approached. We present a simple model based on the number of activated neurons and the strength of activation per neuron that can account for these results. CONCLUSIONS: We show that, for our parametric stimulus set, BOLD activity varied nonmonotonically as a function of how much noise was added to the visual stimuli, unlike the perceptual ability of humans and monkeys to identify such stimuli. This raises important caveats for interpreting fMRI data and demonstrates the importance of assessing not only which neural populations are activated by contrasting conditions during an fMRI study, but also the strength of this activation. This becomes particularly important when using the BOLD signal to make inferences about the relationship between neural activity and behavior.     

The radial bias: a different slant on visual orientation sensitivity in human and nonhuman primates

It is generally assumed that sensitivity to different stimulus orientations is mapped in a globally equivalent fashion across primate visual cortex, at a spatial scale larger than that of orientation columns. However, some evidence predicts instead that radial orientations should produce higher activity than other orientations, throughout visual cortex. Here, this radial orientation bias was robustly confirmed using (1) human psychophysics, plus fMRI in (2) humans and (3) behaving monkeys. In visual cortex, fMRI activity was at least 20% higher in the retinotopic representations of polar angle which corresponded to the radial stimulus orientations (relative to tangential). In a global demonstration of this, we activated complementary retinotopic quadrants of visual cortex by simply changing stimulus orientation, without changing stimulus location in the visual field. This evidence reveals a neural link between orientation sensitivity and the cortical retinotopy, which have previously been considered independent.     

Brain potentials associated with pattern displacement and saccadic eye movements in humans and rhesus monkeys

Visual evoked potentials (VEPs) to the onset of motion of visual patterns and brain responses associated with saccadic eye movements (SRPs) were compared in human subjects and in rhesus monkeys. Three different velocities of pattern motion were employed. In humans, brain responses were recorded from six scalp areas. In monkeys, transcortical recordings were obtained from chronically implanted electrodes in the occipital, temporo-parietal, and frontal areas. In humans there was a clear difference in VEPs to the pattern motion between the anterior (Fz, Cz) and posterior (Pz, Oz) scalp regions. The earliest component was a positive peak at 85 ms at Oz followed by a negativity around 110 ms. In the fronto-central leads the VEP was characterized by a negativity at 145 ms and a subsequent broad positive component around 250 ms. SRP responses differed in the early components from the VEPs to pattern motion but a good correspondence was found in the morphology of the late components of the two types of brain potentials. Furthermore, flashed-on VEPs and SRPs elicited a late positivity of more pronounced amplitude than VEPs to pattern displacement. In monkeys similar findings were found: an early negative component of the pattern-displacement VEP could not be observed in the SRP responses over the visual cortex while the late portion of the SRP waveform was greater than the late positivity of the VEP to motion-onset.     

Collinear interactions and contour integration

The visibility of a local target is influenced by the global configuration of the stimulus. Collinear configurations are a specific case in which facilitation or suppression of the target has been found to be dependent on the contrast threshold of the target. The role of collinear interactions in perceptual grouping, especially in contour integration, is still controversial. In the current study, the role of collinear interactions in noise was investigated using experimental conditions similar to those utilized in studies of contour integration. The contrast detection paradigm in the presence of similar Gabor elements presented in the background was used. The results show that contrast detection threshold of the target alone is increased (suppression) when it is embedded in randomly oriented background elements. However, when the target is flanked by two collinear Gabor elements, the target is facilitated even at higher target contrast levels. Facilitation is not found for orthogonal configurations. The results suggest that the response to a local element in a contour is modified by lateral facilitative and suppressive inputs from elements comprising the smooth contour and randomly oriented background elements, respectively. Thus, detection of elements along a contour should be considered as integration of global neuronal activity rather than as the output of local and individual neurons.     

Evidence for perceptual "trapping" and adaptation in multistable binocular rivalry

When a different pattern is presented to each eye, the perceived image spontaneously alternates between the two patterns (binocular rivalry); the dynamics of these bistable alternations are known to be stochastic. Examining multistable binocular rivalry (involving four dominant percepts), we demonstrated path dependence and on-line adaptation, which were equivalent whether perceived patterns were formed by single-eye dominance or by mixed-eye dominance. The spontaneous perceptual transitions tended to get trapped within a pair of related global patterns (e.g., opponent shapes and symmetric patterns), and during such trapping, the probability of returning to the repeatedly experienced patterns gradually decreased (postselection pattern adaptation). These results suggest that the structure of global shape coding and its adaptation play a critical role in directing spontaneous alternations of visual awareness in perceptual multistability.     

Perception of shape-from-motion in macaque monkeys and humans

Motion is one of the most efficient cues for shape perception. We conducted behavioral experiments to examine how monkeys perceive shapes defined by motion cues and whether they perceive them as humans do. We trained monkeys to perform a shape discrimination task in which shapes were defined by the motion of random dots. Effects of dot density and dot speed on the shape perception of monkeys were examined. Human subjects were also tested using the same paradigm and the test results were compared with those of monkeys. In both monkeys and humans, correct performance rates declined when density or speed of random dots was reduced. Both of them tended to confuse the same combinations of shapes frequently. These results suggest that monkeys and humans perceive shapes defined by motion cues in a similar manner and probably have common neural mechanisms to perceive them. Electronic Publication     

The effect of contour closure on shape perception

We studied psychophysically whether 'contour closure' enhances the accuracy of shape perception. Stimulus configurations (presented on a blank background) always consisted of identical pattern elements, but the positions of the local elements were varied: the global contour shape either contained closure or not. In the first two stimulus conditions (Closure), the oriented pattern elements (Gabor patches) formed a 'closed' rectangular shape composed of either four long lines or four corners. In the third condition (No closure), the global shape was composed of the four corners, but they were outward oriented, and hence they did not form the outline of a closed contour. We measured the precision of shape perception using a discrimination task in which observers judged the aspect ratio of the outline shape i.e. whether the rectangular shape was tall or wide. We found that: (i) shape discrimination was better (more precise) for Closed contours than for Non-closed contours, i.e. the aspect ratio discrimination thresholds were lower for the Closed than Non-closed configurations. The improved performance could not be explained by differences in visibility of the local elements in the two conditions. (ii) For closed contours, shape discrimination was more precise when the local elements were aligned with the global shape, than when the local elements were orthogonal to it.     

A horse's eye view: size and shape discrimination compared with other mammals

Mammals have adapted to a variety of natural environments from underwater to aerial and these different adaptations have affected their specific perceptive and cognitive abilities. This study used a computer-controlled touchscreen system to examine the visual discrimination abilities of horses, particularly regarding size and shape, and compared the results with those from chimpanzee, human and dolphin studies. Horses were able to discriminate a difference of 14% in circle size but showed worse discrimination thresholds than chimpanzees and humans; these differences cannot be explained by visual acuity. Furthermore, the present findings indicate that all species use length cues rather than area cues to discriminate size. In terms of shape discrimination, horses exhibited perceptual similarities among shapes with curvatures, vertical/horizontal lines and diagonal lines, and the relative contributions of each feature to perceptual similarity in horses differed from those for chimpanzees, humans and dolphins. Horses pay more attention to local components than to global shapes.     

Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys

In monkeys, posterior parietal and premotor cortex play an important integrative role in polymodal motion processing. In contrast, our understanding of the convergence of senses in humans is only at its beginning. To test for equivalencies between macaque and human polymodal motion processing, we used functional MRI in normals while presenting moving visual, tactile, or auditory stimuli. Increased neural activity evoked by all three stimulus modalities was found in the depth of the intraparietal sulcus (IPS), ventral premotor, and lateral inferior postcentral cortex. The observed activations strongly suggest that polymodal motion processing in humans and monkeys is supported by equivalent areas. The activations in the depth of IPS imply that this area constitutes the human equivalent of macaque area VIP.     

Effects of Microstimulation in the Anterior Intraparietal Area during Three-Dimensional Shape Categorization

The anterior intraparietal area (AIP) of rhesus monkeys is part of the dorsal visual stream and contains neurons whose visual response properties are commensurate with a role in three-dimensional (3D) shape perception. Neuronal responses in AIP signal the depth structure of disparity-defined 3D shapes, reflect the choices of monkeys while they categorize 3D shapes, and mirror the behavioral variability across different stimulus conditions during 3D-shape categorization. However, direct evidence for a role of AIP in 3D-shape perception has been lacking. We trained rhesus monkeys to categorize disparity-defined 3D shapes and examined AIP''s contribution to 3D-shape categorization by microstimulating in clusters of 3D-shape selective AIP neurons during task performance. We find that microstimulation effects on choices (monkey M1) and reaction times (monkey M1 and M2) depend on the 3D-shape preference of the stimulated site. Moreover, electrical stimulation of the same cells, during either the 3D-shape-categorization task or a saccade task, could affect behavior differently. Interestingly, in one monkey we observed a strong correlation between the strength of choice-related AIP activity (choice probabilities) and the influence of microstimulation on 3D-shape-categorization behavior (choices and reaction time). These findings propose AIP as part of the network responsible for 3D-shape perception. The results also show that the anterior intraparietal cortex contains cells with different tuning properties, i.e. 3D-shape- or saccade-related, that can be dynamically read out depending on the requirements of the task at hand.     

Selectivity of neuronal adaptation does not match response selectivity: a single-cell study of the FMRI adaptation paradigm

fMRI-based adaptation paradigms (fMR-A) have been used to infer neuronal stimulus selectivities in humans. Inferring neuronal selectivities from fMR-A, however, requires an understanding of the relationship between the stimulus selectivity of neuronal adaptation and responses. We studied this relationship by recording single cells in macaque inferior temporal (IT) cortex, an area that shows fMRI adaptation. Repetition of identical object images reduced the responsiveness of single IT neurons. Presentation of an image to which the neuron was unresponsive did not alter the response to a subsequent image that activated the neuron. Successive presentation of two different images to which the neuron responded similarly produced adaptation, but less so than the repeated presentation of an image. The neuronal adaptation at the single-cell level showed a greater degree of stimulus selectivity than the responses. This complicates the interpretation of fMR-A paradigms when inferring neuronal selectivity.     

Collinear Stimuli Induce Local and Cross-Areal Coherence in the Visual Cortex of Behaving Monkeys

Background

Collinear patterns of local visual stimuli are used to study contextual effects in the visual system. Previous studies have shown that proximal collinear flankers, unlike orthogonal, can enhance the detection of a low contrast central element. However, the direct neural interactions between cortical populations processing the individual flanker elements and the central element are largely unknown.

Methodology/Principal Findings

Using voltage-sensitive dye imaging (VSDI) we imaged neural population responses in V1 and V2 areas in fixating monkeys while they were presented with collinear or orthogonal arrays of Gabor patches. We then studied the spatio-temporal interactions between neuronal populations processing individual Gabor patches in the two conditions. Time-frequency analysis of the stimulus-evoked VSDI signal showed power increase mainly in low frequencies, i.e., the alpha band (α; 7–14 Hz). Power in the α-band was more discriminative at a single trial level than other neuronal population measures. Importantly, the collinear condition showed an increased intra-areal (V1-V1 and V2-V2) and inter-areal (V1-V2) α-coherence with shorter latencies than the orthogonal condition, both before and after the removal of the stimulus contribution. α-coherence appeared between discrete neural populations processing the individual Gabor patches: the central element and the flankers.

Conclusions/Significance

Our findings suggest that collinear effects are mediated by synchronization in a distributed network of proximal and distant neuronal populations within and across V1 and V2.     

Position specificity of adaptation-related face aftereffects

It has been shown that prolonged exposure to a human face leads to shape-selective visual aftereffects. It seems that these face-specific aftereffects (FAEs) have multiple components, related to the adaptation of earlier and higher level processing of visual stimuli. The largest magnitude of FAE, using long-term adaptation periods, is usually observed at the retinotopic position of the preceding adaptor stimulus. However, FAE is also detected, to a smaller degree, at other retinal positions in a spatially invariant way and this component depends less on the adaptation duration. Several lines of evidences suggest that while the position-specific FAE involves lower level areas of the ventral processing stream, the position-invariant FAE depends on the activation of higher level face-processing areas and the fusiform gyrus in particular. In the present paper, we summarize the available behavioural, electrophysiological and neuroimaging results regarding the spatial selectivity of FAE and discuss their implications for the visual stability of object representations across saccadic eye movements.     

Satiation in cutaneous saltation.

The extent of cutaneous saltation (the illusory displacement of a tap presented to one skin locus by another tap occurring close in time at another locus) was modified by a "preconditioning" stimulus presented prior to and at a site distant from the saltatory test pattern. The 10-sec vibratory preconditioning (PC) stimulus appears to be analogous to inspection figures that "satiate" the perceptual field in experiments on figural aftereffects, producing changes in the perceived size, position, or shape of subsequent stimuli. The direction of displacement of the saltatory phantom was always away from the locus of the prior PC stimulus, consistent with results observed in studies of visual and kinesthetic aftereffects. Th- amount of repulsion and the rate at which the saltatory phantom returned to its initial position depend on the intensity, locus, and number of PC stimuli. As with figural aftereffects, these results resist explanation by peripheral mechanisms such as adaptation.     

Developmental changes in hierarchical visual stimulus recognition in children aged 5-10 years

Reaction time (RT) and performance accuracy in hierarchical visual stimulus recognition at local and global levels were studied in 95 healthy 5-6, 6-7, 7-8 and 9-10-year-old children and 10 adults. Task performance of all examined subjects, both children and adults, was faster and more accurate during global feature recognition (global advantage effect), with increased RT to incongruent stimuli in local condition (global interference effect). Significant inter-individual differences were found in the youngest group (5-6-year-olds): 7 children from the total number of 37 subjects failed to show the global advantage and global interference effects. Significant progressive shifts in performance accuracy during hierarchical stimulus recognition at both local and global levels were observed in the period between 6-7 and 7-8 years and then between 9-10 years and adulthood. The time course of age-dependent changes in recognition time was different for the global and local features of the hierarchical stimuli: the RT significantly decreased in every successive age group for local feature recognition beginning from 6-7-year-old children, whereas there was no significant difference between 7-8 and 9-10-year-old children in the RT of the recognition of the global feature. In the two younger groups (5-6 and 6-7 years), the stimulus type affected performance in a specific manner: RT increased to both incongruent and neutral stimuli irrespective of the level of the target feature. It was assumed that nonlinear developmental trends in hierarchical stimulus recognition parameters depend on both maturation of visual information processing and development of executive functions, especially those related to selection of relevant signals.     

Adaptation-induced plasticity of orientation tuning in adult visual cortex

A key emergent property of the primary visual cortex (V1) is the orientation selectivity of its neurons. The extent to which adult visual cortical neurons can exhibit changes in orientation selectivity is unknown. Here we use single-unit recording and intrinsic signal imaging in V1 of adult cats to demonstrate systematic repulsive shifts in orientation preference following short-term exposure (adaptation) to one stimulus orientation. In contrast to the common view of adaptation as a passive process by which responses around the adapting orientation are reduced, we show that changes in orientation tuning also occur due to response increases at orientations away from the adapting stimulus. Adaptation-induced orientation plasticity is thus an active time-dependent process that involves network interactions and includes both response depression and enhancement.