Tactile rivalry demonstrated with an ambiguous apparent-motion quartet

When observers view ambiguous visual stimuli, their perception will often alternate between the possible interpretations, a phenomenon termed perceptual rivalry [1]. To induce perceptual rivalry in the tactile domain, we developed a new tactile illusion, based on the visual apparent-motion quartet [2]. Pairs of 200 ms vibrotactile stimuli were applied to the finger pad at intervals separated by 300 ms. The location of each successive stimulus pair alternated between the opposing diagonal corners of the approximately 1 cm(2) stimulation array. This stimulation sequence led all participants to report switches between the perception of motion traveling either up and down or left and right across their fingertip. Adaptation to tactile stimulation biased toward one direction caused subsequent ambiguous stimulation to be experienced in the opposing direction. In contrast, when consecutive trials of ambiguous stimulation were presented, motion was generally perceived in the direction consistent with the motion reported in the previous trial. Voluntary eye movements induced shifts in the tactile perception toward a motion axis aligned along a world-centered coordinate frame. Because the tactile quartet results in switching perceptual states despite unvaried sensory input, it is ideally suited to future studies of the neural processes associated with conscious tactile perception.     

Primary visual cortex activity along the apparent-motion trace reflects illusory perception

The illusion of apparent motion can be induced when visual stimuli are successively presented at different locations. It has been shown in previous studies that motion-sensitive regions in extrastriate cortex are relevant for the processing of apparent motion, but it is unclear whether primary visual cortex (V1) is also involved in the representation of the illusory motion path. We investigated, in human subjects, apparent-motion-related activity in patches of V1 representing locations along the path of illusory stimulus motion using functional magnetic resonance imaging. Here we show that apparent motion caused a blood-oxygenation-level-dependent response along the V1 representations of the apparent-motion path, including regions that were not directly activated by the apparent-motion-inducing stimuli. This response was unaltered when participants had to perform an attention-demanding task that diverted their attention away from the stimulus. With a bistable motion quartet, we confirmed that the activity was related to the conscious perception of movement. Our data suggest that V1 is part of the network that represents the illusory path of apparent motion. The activation in V1 can be explained either by lateral interactions within V1 or by feedback mechanisms from higher visual areas, especially the motion-sensitive human MT/V5 complex.     

Cerebral visual motion blindness: transitory akinetopsia induced by transcranial magnetic stimulation of human area V5.

The perception of visual motion can be selectively and reversibly compromised by transcranial magnetic stimulation (TMS) of a small region of cortex, roughly 1 cm in diameter and corresponding in position to human area V5. The reversible inactivation of a small and specialized visual area which receives its predominant input from area V1 and sends a powerful return (re-entrant) input back to it allowed us to study for the first time the backward influence of area V5 on area V1. In contrast to the complete and temporary visual motion blindness which occurs during stimulation of V5, a less-prominent interference with the perception of visual motion occurs at 70-80 ms after the onset of the visual stimulus when TMS is applied to V1. Because V5 is critical for the perception of coherent motion, and because an intact re-entry of signals from V5 to V1 is essential for the conscious perception of visual motion, the results obtained with stimulation of V1 must be caused by a disruption of the re-entrant signals from V5 to V1.     

Decoding seen and attended motion directions from activity in the human visual cortex

Functional neuroimaging has successfully identified brain areas that show greater responses to visual motion and adapted responses to repeated motion directions. However, such methods have been thought to lack the sensitivity and spatial resolution to isolate direction-selective responses to individual motion stimuli. Here, we used functional magnetic resonance imaging (fMRI) and pattern classification methods to show that ensemble activity patterns in human visual cortex contain robust direction-selective information, from which it is possible to decode seen and attended motion directions. Ensemble activity in areas V1-V4 and MT+/V5 allowed us to decode which of eight possible motion directions the subject was viewing on individual stimulus blocks. Moreover, ensemble activity evoked by single motion directions could effectively predict which of two overlapping motion directions was the focus of the subject's attention and presumably dominant in perception. Our results indicate that feature-based attention can bias direction-selective population activity in multiple visual areas, including MT+/V5 and early visual areas (V1-V4), consistent with gain-modulation models of feature-based attention and theories of early attentional selection. Our approach for measuring ensemble direction selectivity may provide new opportunities to investigate relationships between attentional selection, conscious perception, and direction-selective responses in the human brain.     

The neural basis of centre-surround interactions in visual motion processing

Perception of a moving visual stimulus can be suppressed or enhanced by surrounding context in adjacent parts of the visual field. We studied the neural processes underlying such contextual modulation with fMRI. We selected motion selective regions of interest (ROI) in the occipital and parietal lobes with sufficiently well defined topography to preclude direct activation by the surround. BOLD signal in the ROIs was suppressed when surround motion direction matched central stimulus direction, and increased when it was opposite. With the exception of hMT+/V5, inserting a gap between the stimulus and the surround abolished surround modulation. This dissociation between hMT+/V5 and other motion selective regions prompted us to ask whether motion perception is closely linked to processing in hMT+/V5, or reflects the net activity across all motion selective cortex. The motion aftereffect (MAE) provided a measure of motion perception, and the same stimulus configurations that were used in the fMRI experiments served as adapters. Using a linear model, we found that the MAE was predicted more accurately by the BOLD signal in hMT+/V5 than it was by the BOLD signal in other motion selective regions. However, a substantial improvement in prediction accuracy could be achieved by using the net activity across all motion selective cortex as a predictor, suggesting the overall conclusion that visual motion perception depends upon the integration of activity across different areas of visual cortex.     

MEG responses to the perception of global structure within glass patterns

Background

The perception of global form requires integration of local visual cues across space and is the foundation for object recognition. Here we used magnetoencephalography (MEG) to study the location and time course of neuronal activity associated with the perception of global structure from local image features. To minimize neuronal activity to low-level stimulus properties, such as luminance and contrast, the local image features were held constant during all phases of the MEG recording. This allowed us to assess the relative importance of striate (V1) versus extrastriate cortex in global form perception.

Methodology/Principal Findings

Stimuli were horizontal, rotational and radial Glass patterns. Glass patterns without coherent structure were viewed during the baseline period to ensure neuronal responses reflected perception of structure and not changes in local image features. The spatial distribution of task-related changes in source power was mapped using Synthetic Aperture Magnetometry (SAM), and the time course of activity within areas of maximal power change was determined by calculating time-frequency plots using a Hilbert transform. For six out of eight observers, passive viewing of global structure was associated with a reduction in 10–20 Hz cortical oscillatory power within extrastriate occipital cortex. The location of greatest power change was the same for each pattern type, being close to or within visual area V3a. No peaks of activity were observed in area V1. Time-frequency analyses indicated that neural activity was least for horizontal patterns.

Conclusions

We conclude: (i) visual area V3a is involved in the analysis of global form; (ii) the neural signature for perception of structure, as assessed using MEG, is a reduction in 10–20 Hz oscillatory power; (iii) different neural processes may underlie the perception of horizontal as opposed to radial or rotational structure; and (iv) area V1 is not strongly activated by global form in Glass patterns.     

MPI CyberMotion Simulator: implementation of a novel motion simulator to investigate multisensory path integration in three dimensions

Path integration is a process in which self-motion is integrated over time to obtain an estimate of one's current position relative to a starting point (1). Humans can do path integration based exclusively on visual (2-3), auditory (4), or inertial cues (5). However, with multiple cues present, inertial cues - particularly kinaesthetic - seem to dominate (6-7). In the absence of vision, humans tend to overestimate short distances (<5 m) and turning angles (<30°), but underestimate longer ones (5). Movement through physical space therefore does not seem to be accurately represented by the brain. Extensive work has been done on evaluating path integration in the horizontal plane, but little is known about vertical movement (see (3) for virtual movement from vision alone). One reason for this is that traditional motion simulators have a small range of motion restricted mainly to the horizontal plane. Here we take advantage of a motion simulator (8-9) with a large range of motion to assess whether path integration is similar between horizontal and vertical planes. The relative contributions of inertial and visual cues for path navigation were also assessed. 16 observers sat upright in a seat mounted to the flange of a modified KUKA anthropomorphic robot arm. Sensory information was manipulated by providing visual (optic flow, limited lifetime star field), vestibular-kinaesthetic (passive self motion with eyes closed), or visual and vestibular-kinaesthetic motion cues. Movement trajectories in the horizontal, sagittal and frontal planes consisted of two segment lengths (1st: 0.4 m, 2nd: 1 m; ±0.24 m/s(2) peak acceleration). The angle of the two segments was either 45° or 90°. Observers pointed back to their origin by moving an arrow that was superimposed on an avatar presented on the screen. Observers were more likely to underestimate angle size for movement in the horizontal plane compared to the vertical planes. In the frontal plane observers were more likely to overestimate angle size while there was no such bias in the sagittal plane. Finally, observers responded slower when answering based on vestibular-kinaesthetic information alone. Human path integration based on vestibular-kinaesthetic information alone thus takes longer than when visual information is present. That pointing is consistent with underestimating and overestimating the angle one has moved through in the horizontal and vertical planes respectively, suggests that the neural representation of self-motion through space is non-symmetrical which may relate to the fact that humans experience movement mostly within the horizontal plane.     

Implications on visual apperception: Energy, duration, structure and synchronization

Although primary visual cortex (V1 or striate) activity per se is not sufficient for visual apperception (normal conscious visual experiences and conscious functions such as detection, discrimination, and recognition), the same is also true for extrastriate visual areas (such as V2, V3, V4/V8/VO, V5/M5/MST, IT, and GF). In the lack of V1 area, visual signals can still reach several extrastriate parts but appear incapable of generating normal conscious visual experiences. It is scarcely emphasized in the scientific literature that conscious perceptions and representations must have also essential energetic conditions. These energetic conditions are achieved by spatiotemporal networks of dynamic mitochondrial distributions inside neurons. However, the highest density of neurons in neocortex (number of neurons per degree of visual angle) devoted to representing the visual field is found in retinotopic V1. It means that the highest mitochondrial (energetic) activity can be achieved in mitochondrial cytochrome oxidase-rich V1 areas. Thus, V1 bear the highest energy allocation for visual representation.In addition, the conscious perceptions also demand structural conditions, presence of adequate duration of information representation, and synchronized neural processes and/or ‘interactive hierarchical structuralism.’ For visual apperception, various visual areas are involved depending on context such as stimulus characteristics such as color, form/shape, motion, and other features. Here, we focus primarily on V1 where specific mitochondrial-rich retinotopic structures are found; we will concisely discuss V2 where smaller riches of these structures are found. We also point out that residual brain states are not fully reflected in active neural patterns after visual perception. Namely, after visual perception, subliminal residual states are not being reflected in passive neural recording techniques, but require active stimulation to be revealed.     

Delayed perceptual awareness in rapid perceptual decisions

The flourishing of studies on the neural correlates of decision-making calls for an appraisal of the relation between perceptual decisions and conscious perception. By exploiting the long integration time of noisy motion stimuli, and by forcing human observers to make difficult speeded decisions--sometimes a blind guess--about stimulus direction, we traced the temporal buildup of motion discrimination capability and perceptual awareness, as assessed trial by trial through direct rating. We found that both increased gradually with motion coherence and viewing time, but discrimination was systematically leading awareness, reaching a plateau much earlier. Sensitivity and criterion changes contributed jointly to the slow buildup of perceptual awareness. It made no difference whether motion discrimination was accomplished by saccades or verbal responses. These findings suggest that perceptual awareness emerges on the top of a developing or even mature perceptual decision. We argue that the middle temporal (MT) cortical region does not confer us the full phenomenic depth of motion perception, although it may represent a precursor stage in building our subjective sense of visual motion.     

Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain

There is much evidence in primates' visual processing for distinct mechanisms involved in object recognition and encoding object position and motion, which have been identified with 'ventral' and 'dorsal' streams, respectively, of the extra-striate visual areas [1] [2] [3]. This distinction may yield insights into normal human perception, its development and pathology. Motion coherence sensitivity has been taken as a test of global processing in the dorsal stream [4] [5]. We have proposed an analogous 'form coherence' measure of global processing in the ventral stream [6]. In a functional magnetic resonance imaging (fMRI) experiment, we found that the cortical regions activated by form coherence did not overlap with those activated by motion coherence in the same individuals. Areas differentially activated by form coherence included regions in the middle occipital gyrus, the ventral occipital surface, the intraparietal sulcus, and the temporal lobe. Motion coherence activated areas consistent with those previously identified as V5 and V3a, the ventral occipital surface, the intraparietal sulcus, and temporal structures. Neither form nor motion coherence activated area V1 differentially. Form and motion foci in occipital, parietal, and temporal areas were nearby but showed almost no overlap. These results support the idea that form and motion coherence test distinct functional brain systems, but that these do not necessarily correspond to a gross anatomical separation of dorsal and ventral processing streams.     

Stability of cortical responses and the statistics of natural scenes.

The primary visual cortex (V1) of higher mammals contains maps of stimulus features; how these maps influence vision remains unknown. We have examined the functional significance of an asymmetry in the orientation map in cat V1, i.e., the fact that a larger area of V1 is preferentially activated by vertical and horizontal contours than by contours at oblique orientations. Despite the fact that neurons tuned to cardinal and oblique orientations have indistinguishable tuning characteristics, cardinal neurons remain more stable in their response properties after selective perturbation induced by adaptation. Similarly, human observers report different adaptation-induced changes in orientation tuning between cardinal and oblique axes. We suggest that the larger cortical area devoted to cardinal orientations imposes stability on the processing of cardinal contours during visual perception, by retaining invariant cortical responses along cardinal axes.     

Perception matches selectivity in the human anterior color center

Human ventral cortex contains at least two visual areas selective for color [1]: a posterior center in the lingual gyrus labeled V4 [2-4], V8 [5], or VO-1 [6] and an anterior center in the medial fusiform that has been labeled V4alpha[3, 4]. We examined the properties of the anterior color center using electrical recording and electrical stimulation in a subject with an electrode implanted over the anterior color center, as determined with BOLD fMRI in the same subject. Presentation of visual stimuli evoked local field potentials from the electrode. Consistent with fMRI, the potentials were larger for chromatic than achromatic stimuli. The potentials differed depending on stimulus color, with blue-purple colors evoking the largest response. The spatial receptive field of the electrode was central/parafoveal with a contralateral bias. In the absence of a visual stimulus, electrical stimulation of the electrode produced an artificial visual percept of a blue-purple color near the center of gaze. These results provide direct evidence of a tight link between selectivity and perception in ventral temporal cortex. Electrical stimulation of the anterior color center is sufficient to produce the conscious percept of a color whose identity is determined by the selectivity of the stimulated neurons.     

Dissociation of neuronal and psychophysical responses to local and global motion

Most neurons in cortical area MT (V5) are strongly direction selective, and their activity is closely associated with the perception of visual motion. These neurons have large receptive fields built by combining inputs with smaller receptive fields that respond to local motion. Humans integrate motion over large areas and can perceive what has been referred to as global motion. The large size and direction selectivity of MT receptive fields suggests that MT neurons may represent global motion. We have explored this possibility by measuring responses to a stimulus in which the directions of simultaneously presented local and global motion are independently controlled. Surprisingly, MT responses depended only on the local motion and were unaffected by the global motion. Yet, under similar conditions, human observers perceive global motion and are impaired in discriminating local motion. Although local motion perception might depend on MT signals, global motion perception depends on mechanisms qualitatively different from those in MT. Motion perception therefore does not depend on a single cortical area but reflects the action and interaction of multiple brain systems.     

Integration of Motion Responses Underlying Directional Motion Anisotropy in Human Early Visual Cortical Areas

Recent imaging studies have reported directional motion biases in human visual cortex when perceiving moving random dot patterns. It has been hypothesized that these biases occur as a result of the integration of motion detector activation along the path of motion in visual cortex. In this study we investigate the nature of such motion integration with functional MRI (fMRI) using different motion stimuli. Three types of moving random dot stimuli were presented, showing either coherent motion, motion with spatial decorrelations or motion with temporal decorrelations. The results from the coherent motion stimulus reproduced the centripetal and centrifugal directional motion biases in V1, V2 and V3 as previously reported. The temporally decorrelated motion stimulus resulted in both centripetal and centrifugal biases similar to coherent motion. In contrast, the spatially decorrelated motion stimulus resulted in small directional motion biases that were only present in parts of visual cortex coding for higher eccentricities of the visual field. In combination with previous results, these findings indicate that biased motion responses in early visual cortical areas most likely depend on the spatial integration of a simultaneously activated motion detector chain.     

Transitions between central and peripheral vision create spatial/temporal distortions: a hypothesis concerning the perceived break of the curveball

Background

The human visual system does not treat all parts of an image equally: the central segments of an image, which fall on the fovea, are processed with a higher resolution than the segments that fall in the visual periphery. Even though the differences between foveal and peripheral resolution are large, these differences do not usually disrupt our perception of seamless visual space. Here we examine a motion stimulus in which the shift from foveal to peripheral viewing creates a dramatic spatial/temporal discontinuity.

Methodology/Principal Findings

The stimulus consists of a descending disk (global motion) with an internal moving grating (local motion). When observers view the disk centrally, they perceive both global and local motion (i.e., observers see the disk''s vertical descent and the internal spinning). When observers view the disk peripherally, the internal portion appears stationary, and the disk appears to descend at an angle. The angle of perceived descent increases as the observer views the stimulus from further in the periphery. We examine the first- and second-order information content in the display with the use of a three-dimensional Fourier analysis and show how our results can be used to describe perceived spatial/temporal discontinuities in real-world situations.

Conclusions/Significance

The perceived shift of the disk''s direction in the periphery is consistent with a model in which foveal processing separates first- and second-order motion information while peripheral processing integrates first- and second-order motion information. We argue that the perceived distortion may influence real-world visual observations. To this end, we present a hypothesis and analysis of the perception of the curveball and rising fastball in the sport of baseball. The curveball is a physically measurable phenomenon: the imbalance of forces created by the ball''s spin causes the ball to deviate from a straight line and to follow a smooth parabolic path. However, the curveball is also a perceptual puzzle because batters often report that the flight of the ball undergoes a dramatic and nearly discontinuous shift in position as the ball nears home plate. We suggest that the perception of a discontinuous shift in position results from differences between foveal and peripheral processing.     

Responses to lightness variations in early human visual cortex

Lightness is the apparent reflectance of a surface, and it depends not only on the actual luminance of the surface but also on the context in which the surface is viewed [1-10]. The cortical mechanisms of lightness processing are largely unknown, and the role of early cortical areas is still a matter of debate [11-17]. We studied the cortical responses to lightness variations in early stages of the human visual system with functional magnetic resonance imaging (fMRI) while observers were performing a demanding fixation task. The set of dynamically presented visual stimuli included the rectangular version of the classic Craik-O'Brien stimulus [3, 18, 19] and a variant that led to a weaker lightness effect, as well as a pattern with actual luminance variations. We found that the cortical activity in retinotopic areas, including the primary visual cortex (V1), is correlated with context-dependent lightness variations.     

The visual cortical association field: A Gestalt concept or a psychophysiological entity?

The receptive field of a visual neurone is classically defined as the region of space (or retina) where a visual stimulus evokes a change in its firing activity. Intracellular recordings in cat area 17 show that the visually evoked synaptic integration field extends over a much larger area than that established on the basis of spike activity. Synaptic depolarizing (dominant excitation) responses decrease in strength for stimuli that are flashed at increasing distances away from the centre of the discharge field, while their onset latency increases. A detailed spatio-temporal analysis of these electrophysiological data shows that subthreshold synaptic responses observed in the 'silent' surround of cortical receptive fields result from the intracortical spread of activation waves carried by slowly conducting horizontal axons within primary visual cortex. They also predict that a perceptual facilitation may occur when feedforward activation produced by the motion signal in the retina travels in phase in the primary visual cortex with the visually induced spread of horizontal activation. A psychophysical correlate has been obtained in humans, showing that apparent motion produced by a sequence of co-linear Gabor patches, known to preferentially activate V1 orientation selective cells, are perceived by human observers as much faster than non co-linear sequences of the same physical speed.     

Modeling spatial integration in the ocular following response using a probabilistic framework

The machinery behind the visual perception of motion and the subsequent sensori-motor transformation, such as in ocular following response (OFR), is confronted to uncertainties which are efficiently resolved in the primate's visual system. We may understand this response as an ideal observer in a probabilistic framework by using Bayesian theory [Weiss, Y., Simoncelli, E.P., Adelson, E.H., 2002. Motion illusions as optimal percepts. Nature Neuroscience, 5(6), 598-604, doi:10.1038/nn858] which we previously proved to be successfully adapted to model the OFR for different levels of noise with full field gratings. More recent experiments of OFR have used disk gratings and bipartite stimuli which are optimized to study the dynamics of center-surround integration. We quantified two main characteristics of the spatial integration of motion: (i) a finite optimal stimulus size for driving OFR, surrounded by an antagonistic modulation and (ii) a direction selective suppressive effect of the surround on the contrast gain control of the central stimuli [Barthélemy, F.V., Vanzetta, I., Masson, G.S., 2006. Behavioral receptive field for ocular following in humans: dynamics of spatial summation and center-surround interactions. Journal of Neurophysiology, (95), 3712-3726, doi:10.1152/jn.00112.2006]. Herein, we extended the ideal observer model to simulate the spatial integration of the different local motion cues within a probabilistic representation. We present analytical results which show that the hypothesis of independence of local measures can describe the spatial integration of the motion signal. Within this framework, we successfully accounted for the contrast gain control mechanisms observed in the behavioral data for center-surround stimuli. However, another inhibitory mechanism had to be added to account for suppressive effects of the surround.     

A novel interhemispheric interaction: modulation of neuronal cooperativity in the visual areas

Background

The cortical representation of the visual field is split along the vertical midline, with the left and the right hemi-fields projecting to separate hemispheres. Connections between the visual areas of the two hemispheres are abundant near the representation of the visual midline. It was suggested that they re-establish the functional continuity of the visual field by controlling the dynamics of the responses in the two hemispheres.

Methods/Principal Findings

To understand if and how the interactions between the two hemispheres participate in processing visual stimuli, the synchronization of responses to identical or different moving gratings in the two hemi-fields were studied in anesthetized ferrets. The responses were recorded by multiple electrodes in the primary visual areas and the synchronization of local field potentials across the electrodes were analyzed with a recent method derived from dynamical system theory. Inactivating the visual areas of one hemisphere modulated the synchronization of the stimulus-driven activity in the other hemisphere. The modulation was stimulus-specific and was consistent with the fine morphology of callosal axons in particular with the spatio-temporal pattern of activity that axonal geometry can generate.

Conclusions/Significance

These findings describe a new kind of interaction between the cerebral hemispheres and highlight the role of axonal geometry in modulating aspects of cortical dynamics responsible for stimulus detection and/or categorization.     

Vertical disparity, egocentric distance and stereoscopic depth constancy: a new interpretation

There has long been a problem concerning the presence in the visual cortex of binocularly activated cells that are selective for vertical stimulus disparities because it is generally believed that only horizontal disparities contribute to stereoscopic depth perception. The accepted view is that stereoscopic depth estimates are only relative to the fixation point and that independent information from an extraretinal source is needed to scale for absolute or egocentric distance. Recently, however, theoretical computations have shown that egocentric distance can be estimated directly from vertical disparities without recourse to extraretinal sources. There has been little impetus to follow up these computations with experimental observations, because the vertical disparities that normally occur between the images in the two eyes have always been regarded as being too small to be of significance for visual perception and because experiments have consistently shown that our conscious appreciation of egocentric distance is rather crude and unreliable. Nevertheless, the veridicality of stereoscopic depth constancy indicates that accurate distance information is available to the visual system and that the information about egocentric distance and horizontal disparity are processed together so as to continually recalibrate the horizontal disparity values for different absolute distances. Computations show that the recalibration can be based directly on vertical disparities without the need for any intervening estimates of absolute distance. This may partly explain the relative crudity of our conscious appreciation of egocentric distance. From published data it has been possible to calculate the magnitude of the vertical disparities that the human visual system must be able to discriminate in order for depth constancy to have the observed level of veridicality. From published data on the induced effect it has also been possible to calculate the threshold values for the detection of vertical disparities by the visual system. These threshold values are smaller than those needed to provide for the recalibration of the horizontal disparities in the interests of veridical depth constancy. An outline is given of the known properties of the binocularly activated cells in the striate cortex that are able to discriminate and assess the vertical disparities. Experiments are proposed that should validate, or otherwise, the concepts put forward in this paper.