Effect of spatial context on perceived walking direction.

Contextual modulation occurs for many aspects of high-level vision but is relatively unexplored for the perception of walking direction. In a recent study, we observed an effect of the temporal context on perceived walking direction. Here, we examined the spatial contextual modulation by measuring the perceived direction of a target point-light walker in the presence of two flanker walkers, one on each side. Experiment 1 followed a within-subjects design. Participants (n = 30) completed a spatial context task by judging the walking direction of the target in 13 different conditions: a walker alone in the center or with two flanking walkers either intact or scrambled at a flanker deviation of ±15°, ±30°, or ±45°. For comparison, participants completed an adaptation task where they reported the walking direction of a target after adaptation to ±30° walking direction. We found the expected repulsive effects in the adaptation task but attractive effects in the spatial context task. In Experiment 2 (n = 40), we measured the tuning of spatial contextual modulation across a wide range of flanker deviation magnitudes ranging from 15° to 165° in 15° intervals. Our results showed significant attractive effects across a wide range of flanker walking directions with the peak effect at around 30°. The assimilative versus repulsive effects of spatial contextual modulation and temporal adaptation suggest dissociable neural mechanisms, but they may operate on the same population of sensory channels coding for walking direction, as evidenced by similarity in the peak tuning across the walking direction of the inducers.

The long and short of it? A novel geometric illusion.

Here we present what we believe to be a novel geometric illusion where identical lines are perceived as being of differing lengths. Participants were asked to report which of the two parallel rows of horizontal lines contained the longer individual lines (two lines on one row and 15 on the other). Using an adaptive staircase we adjusted the length of the lines on the row containing two to estimate the point of subjective equality (PSE). At the PSE, the two lines were consistently shorter than the row containing the fixed length of 15 lines demonstrating a disparity in perceived length such that lines of identical length are perceived as longer in a row of two than in a row of 15. The illusion magnitude was unaffected by which row was presented above the other. Additionally, the effect persisted when using one as opposed to two test lines, and when the line stimuli on both rows were presented with alternating luminance polarity the illusion magnitude decreased, but was not abolished. The data indicate a robust geometric illusion that may be modulated by perceptual grouping processes.

Detection of Mooney faces is robust to image asymmetries produced by illumination.

Face detection relies on the visual features that are shared across different faces. An important component of the basic spatial configuration of a face is symmetry around the vertical midline. Although human faces are structurally symmetrical, they can be asymmetrical in an image due to the direction of lighting or the position of the face. In the experiments presented here, we examined how face detection from simple contrast patterns that occur across the face is affected by the image asymmetries associated with variations in the horizontal lighting direction. We presented observers with two-tone images of faces (Mooney faces) that isolated the unique pattern of contrast in the shading and shadows on a face, illuminated from a wide range of horizontal directions. In two experiments, we found that face detection is surprisingly robust to these lighting changes, with sensitivity in discriminating between face and non-face patterns reduced only at the most extreme lighting directions. This tolerance to changes in the horizontal lighting direction depended partly on the orientation of the face, vertical lighting direction, and contrast polarity. Our results provide insight into how contrast cues produced by shading and shadows occurring across the facial surface are utilized by the visual system to detect human faces.

Spatial selectivity in adaptation to gaze direction.

A person's focus of attention is conveyed by the direction of their eyes and face, providing a simple visual cue fundamental to social interaction. A growing body of research examines the visual mechanisms that encode the direction of another person's gaze as we observe them. Here we investigate the spatial receptive field properties of these mechanisms, by testing the spatial selectivity of sensory adaptation to gaze direction. Human observers were adapted to faces with averted gaze presented in one visual hemifield, then tested in their perception of gaze direction for faces presented in the same or opposite hemifield. Adaptation caused strong, repulsive perceptual aftereffects, but only for faces presented in the same hemifield as the adapter. This occurred even though adapting and test stimuli were in the same external location across saccades. Hence, there was clear evidence for retinotopic adaptation and a relative lack of either spatiotopic or spatially invariant adaptation. These results indicate that adaptable representations of gaze direction in the human visual system have retinotopic spatial receptive fields. This strategy of coding others' direction of gaze with positional specificity relative to one's own eye position may facilitate key functions of gaze perception, such as socially cued shifts in visual attention.

The Mesolimbic Dopamine Activity Signatures of Relapse to Alcohol-Seeking.

The mesolimbic dopamine system comprises distinct compartments supporting different functions in learning and motivation. Less well understood is how complex addiction-related behaviors emerge from activity patterns across these compartments. Here we show how different forms of relapse to alcohol-seeking in male rats are assembled from activity across the VTA and the nucleus accumbens. First, we used chemogenetic approaches to show a causal role for VTA TH neurons in two forms of relapse to alcohol-seeking: renewal (context-induced reinstatement) and reacquisition. Then, using gCaMP fiber photometry of VTA TH neurons, we identified medial and lateral VTA TH neuron activity profiles during self-administration, renewal, and reacquisition. Next, we used optogenetic inhibition of VTA TH neurons to show distinct causal roles for VTA subregions in distinct forms of relapse. We then used dLight fiber photometry to measure dopamine binding across the ventral striatum (medial accumbens shell, accumbens core, lateral accumbens shell) and showed complex and heterogeneous profiles of dopamine binding during self-administration and relapse. Finally, we used representational similarity analysis to identify mesolimbic dopamine signatures of self-administration, extinction, and relapse. Our results show that signatures of relapse can be identified from heterogeneous activity profiles across the mesolimbic dopamine system and that these signatures are unique for different forms of relapse.SIGNIFICANCE STATEMENT It is axiomatic that the actions of dopamine are critical to drug addiction. Yet how relapse to drug-seeking is assembled from activity across the mesolimbic dopamine system is poorly understood. Here we show how relapse to alcohol-seeking relates to activity in specific VTA and accumbens compartments, how these change for different forms of relapse, and how relapse-associated activity relates to activity during self-administration and extinction. We report the mesolimbic dopamine activity signatures for relapse and show that these signatures are unique for different forms of relapse.

Paraventricular Thalamus Controls Behavior during Motivational Conflict.

Decision-making often involves motivational conflict because of the competing demands of approach and avoidance for a common resource: behavior. This conflict must be resolved as a necessary precursor for adaptive behavior. Here we show a role for the paraventricular thalamus (PVT) in behavioral control during motivational conflict. We used Pavlovian counterconditioning in male rats to establish a conditioned stimulus (CS) as a signal for reward (or danger) and then transformed the same CS into a signal for danger (or reward). After such training, the CS controls conflicting appetitive and aversive behaviors. To assess PVT involvement in conflict, we injected an adeno-associated virus (AAV) expressing the genetically encoded Ca2+ indicator GCaMP and used fiber photometry to record population PVT Ca2+ signals. We show distinct profiles of responsivity across the anterior-posterior axis of PVT during conflict, including an ordinal relationship between posterior PVT CS responses and behavior strength. To study the causal role of PVT in behavioral control during conflict, we injected AAV expressing the inhibitory hM4Di DREADD and determined the effects of chemogenetic PVT inhibition on behavior. We show that chemogenetic inhibition across the anterior-posterior axis of the PVT, but not anterior or posterior PVT alone, disrupts arbitration between appetitive and aversive behaviors when they are in conflict but has no effect when these behaviors are assessed in isolation. Together, our findings identify PVT as central to behavioral control during motivational conflict.SIGNIFICANCE STATEMENT Animals, including humans, approach attractive stimuli and avoid aversive ones. However, they frequently face conflict when the demands of approach and avoidance are incompatible. Resolution of this conflict is fundamental to adaptive behavior. Here we show a role for the paraventricular thalamus, a nucleus of the dorsal midline thalamus, in the arbitration of appetitive and aversive behavior during motivational conflict.

Face Pareidolia Recruits Mechanisms for Detecting Human Social Attention.

Face pareidolia is the phenomenon of seeing facelike structures in everyday objects. Here, we tested the hypothesis that face pareidolia, rather than being limited to a cognitive or mnemonic association, reflects the activation of visual mechanisms that typically process human faces. We focused on sensory cues to social attention, which engage cell populations in temporal cortex that are susceptible to habituation effects. Repeated exposure to "pareidolia faces" that appear to have a specific direction of attention causes a systematic bias in the perception of where human faces are looking, indicating that overlapping sensory mechanisms are recruited when we view human faces and when we experience face pareidolia. These cross-adaptation effects are significantly reduced when pareidolia is abolished by removing facelike features from the objects. These results indicate that face pareidolia is essentially a perceptual phenomenon, occurring when sensory input is processed by visual mechanisms that have evolved to extract specific social content from human faces.

Temporal cueing enhances neuronal and behavioral discrimination performance in rat whisker system.

Since sensory systems operate with a finite quantity of processing resources, an animal would benefit from prioritizing processing of sensory stimuli within a time window that is expected to provide key information. This behavioral manifestation of such prioritization is known as attention. Here, we investigate attention with temporal cueing and its neuronal correlates in the rat primary vibrissal somatosensory (vS1) cortex. Rats were trained in a simple whisker vibration detection task. A vibration was presented at one of two spatial locations (left or right), sometimes after an unknown time interval and sometimes after receiving an auditory cue. The auditory cue provided temporal but not spatial information about the vibration. We found that for all rats ( n = 6), the auditory cue consistently enhanced detection of the vibration stimulus. Neuronal activity in vS1 cortex reflected the observed behavioral enhancement from temporal cueing with single units responded differentially to the whisker vibration stimulus when it was temporally predicted by the auditory cue, exhibiting an enhanced signal-to-noise ratio. Our findings indicate that rats are capable of prioritizing processing within a specified time window and provide evidence that the primary sensory cortex may participate in the temporal allocation of resources. NEW & NOTEWORTHY We demonstrate a novel paradigm of temporal cueing in rats. In a two-alternative whisker detection task, an auditory cue provided information about the timing of the stimulus but not the correct choice. In the presence of cue, detection was faster and more accurate, and neuronal activity from the primary somatosensory cortex revealed enhanced representation of vibrations. These results thus establish the rat as an alternative model organism to primates for studying temporal attention.

Gazing into space: Systematic biases in determining another's fixation distance from gaze vergence in upright and inverted faces.

The eyes of others play a crucial role in social interactions, providing information such as the focus of another's attention and their current thoughts and emotions. Although much research has focused on understanding how we perceive gaze direction, little has been done on gaze vergence, which can potentially yield information about the distance of another's fixation. Here, we presented participants with synthetic faces in a stereoscopically simulated 3-D environment to determine the absolute fixation distance at which they perceived a face to be gazing. The results showed an underestimation in fixation distance for downward-averted gaze and a limit in discrimination of gaze vergence beyond 35 cm. For inverted faces, fixation distance for gaze vergence in the lower visual field (corresponding to the avatar's upwards gaze) was underestimated, suggesting that our bias to underestimate others' fixation distance may rely on a viewer-centered, egocentric representation of interpersonal space.

Correlates of Perceptual Orientation Biases in Human Primary Visual Cortex.

Vision can be considered as a process of probabilistic inference. In a Bayesian framework, perceptual estimates from sensory information are combined with prior knowledge, with a stronger influence of the prior when the sensory evidence is less certain. Here, we explored the behavioral and neural consequences of manipulating stimulus certainty in the context of orientation processing. First, we asked participants to judge whether a stimulus was oriented closer to vertical or the clockwise primary oblique (45°) for two stimulus types (spatially filtered noise textures and sinusoidal gratings) and three manipulations of certainty (orientation bandwidth, contrast, and duration). We found that participants consistently had a bias toward reporting orientation as closer to 45° during conditions of high certainty and that this bias was reduced when sensory evidence was less certain. Second, we measured event-related fMRI BOLD responses in human primary visual cortex (V1) and manipulated certainty via stimulus contrast (100% vs 3%). We then trained a multivariate classifier on the pattern of responses in V1 to cardinal and primary oblique orientations. We found that the classifier showed a bias toward classifying orientation as oblique at high contrast but categorized a wider range of orientations as cardinal for low-contrast stimuli. Orientation classification based on data from V1 thus paralleled the perceptual biases revealed through the behavioral experiments. This pattern of bias cannot be explained simply by a prior for cardinal orientations.SIGNIFICANCE STATEMENT Our perception of the world around us is biased through prior expectations rather than necessarily reflecting the true state of our environment. Here, we investigate biases in the visual processing of spatial orientation to understand how prior expectations and current sensory information interact to generate a percept. By degrading visual input in various ways, we are able to quantify the extent to which prior experience affects both perceptual judgments and neural responses in the human visual system. We observe systematic biases in the perception of orientation that correlate with the pattern of activity in the primary visual cortex of the human brain. These results indicate that prior expectations influence neural processing right from the earliest stage of the cortical hierarchy.

Directional Limits on Motion Transparency Assessed Through Colour-Motion Binding.

Motion-defined transparency is the perception of two or more distinct moving surfaces at the same retinal location. We explored the limits of motion transparency using superimposed surfaces of randomly positioned dots defined by differences in motion direction and colour. In one experiment, dots were red or green and we varied the proportion of dots of a single colour that moved in a single direction ('colour-motion coherence') and measured the threshold direction difference for discriminating between two directions. When colour-motion coherences were high (e.g., 90% of red dots moving in one direction), a smaller direction difference was required to correctly bind colour with direction than at low coherences. In another experiment, we varied the direction difference between the surfaces and measured the threshold colour-motion coherence required to discriminate between them. Generally, colour-motion coherence thresholds decreased with increasing direction differences, stabilising at direction differences around 45°. Different stimulus durations were compared, and thresholds were higher at the shortest (150 ms) compared with the longest (1,000 ms) duration. These results highlight different yet interrelated aspects of the task and the fundamental limits of the mechanisms involved: the resolution of narrowly separated directions in motion processing and the local sampling of dot colours from each surface.

Influence of head orientation on perceived gaze direction and eye-region information.

Using synthetic 3D head and eye models, we examined the relationship between perceived gaze direction and the information within the image eye region across changes in head orientation. For each stimulus head and eye orientation, we rendered gray-scale images with realistic pigmentation and shading, and two-tone images depicting the regions corresponding to the iris, pupil, or eye-opening. Behavioural experiments using the gray-scale images as stimuli showed that perceived gaze direction was more strongly biased opposite to head orientation (repulsive effect) in the far-eye visible condition than in the near-eye visible condition. This trend occurred regardless of whether or not the whole face was visible, suggesting that the repulsive effect arose based on eye-region information. Consistent with this, geometrical analysis of the image eye region using the two-tone images revealed that the relative position of the iris and pupil of the far eye shifted opposite to head orientation more than that of the near eye. In addition, our findings regarding the pattern of the influence of head orientation suggest that estimation of the relative iris/pupil position may be achieved through a process of amodal completion of the whole iris behind the eyelid. Additional geometrical analysis of simulated images revealed situations where a greater repulsive effect for the far eye, as found here, is likely to be observed.

Cortical suppression in human primary visual cortex predicts individual differences in illusory tilt perception.

Neural responses to visual stimuli are modulated by spatial and temporal context. For example, in primary visual cortex (V1), responses to an oriented target stimulus will be suppressed when embedded within an oriented surround stimulus. This suppression is orientation-specific, with the largest suppression observed when stimuli in the neuron's classical receptive field and surround are of similar orientation. In human psychological experiments, the tilt illusion and tilt aftereffect demonstrate an effect of context on perceived orientation of a target stimulus. Similar to the neurophysiological data, the strength of these effects is modulated by the orientation difference between the target stimulus and context. It has been hypothesized that the neural mechanism underlying both the tilt illusion and tilt aftereffect involves orientation-tuned inhibition in V1. However, to date there is no direct evidence linking human perception of these illusions with measurements of inhibition from human visual cortex. Here, we measured context-induced suppression of neural responses in human visual cortex using functional magnetic resonance imaging (fMRI). In the same participants, we also measured magnitudes of their tilt illusion and tilt aftereffect. Our data revealed a significant relationship between the magnitude of neural suppression in V1 and size of the tilt illusion and tilt aftereffect. That is, participants who showed stronger blood oxygenation level dependent (BOLD) suppression in V1 also perceived stronger shifts in illusory tilt. This agreement between perception and neural responses in human V1 suggests a shared inhibitory mechanism that mediates both spatial and temporal effects of context in human perception.

Functional Mechanisms Encoding Others' Direction of Gaze in the Human Nervous System.

The direction of others' gaze is a strong social signal to their intentions and future behavior. Pioneering electrophysiological research identified cell populations in the primate visual cortex that are tuned to specific directions of observed gaze, but the functional architecture of this system is yet to be precisely specified. Here, we develop a computational model of how others' gaze direction is flexibly encoded across sensory channels within the gaze system. We incorporate the divisive normalization of sensory responses-a computational mechanism that is thought to be widespread in sensory systems but has not been examined in the context of social vision. We demonstrate that the operation of divisive normalization in the gaze system predicts a surprising and distinctive pattern of perceptual changes after sensory adaptation to gaze stimuli and find that these predictions closely match the psychophysical effects of adaptation in human observers. We also find that opponent coding, broadband multichannel, and narrowband multichannel models of sensory coding make distinct predictions regarding the effects of adaptation in a normalization framework and find evidence in favor of broadband multichannel coding of gaze. These results reveal the functional principles that govern the neural encoding of gaze direction and support the notion that divisive normalization is a canonical feature of nervous system function. Moreover, this research provides a strong foundation for testing recent computational theories of neuropsychiatric conditions in which gaze processing is compromised, such as autism and schizophrenia.

Probing the Characteristics of Colour-Motion Binding and Its Dependence on Persistent Surface Segregation.

Identifying the spatial and temporal characteristics of visual feature binding is a remaining challenge in the science of perception. Within the feature-binding literature, disparate findings have suggested the existence of more than one feature-binding mechanism with differing temporal resolutions. For example, one surprising result is that temporal alternations between two different feature pairings of colour and motion (e.g., orange dots moving left with blue dots moving right) support accurate conjunction discrimination at alternation frequencies of around 10 Hz and greater. However, at lower alternation frequencies around 5 Hz, conjunction discrimination falls to chance. To further investigate this effect, we present two experiments that probe the stimulus characteristics that facilitate or impede feature binding. Using novel manipulations of random dot kinematograms, we identify that facilitating surface representations through temporal integration can enable accurate conjunction discrimination at both intermediate and high alternation frequencies. We also offer a neurally plausible evidence accumulator model to describe these results, removing the need to suggest multiple binding mechanisms acting at different timescales. In effect, we propose a single, flexible binding process, whereby the relatively low temporal resolution for binding features can be circumvented by extracting them from rapidly formed and persistent surface representations.

Testing the dual-route model of perceived gaze direction: Linear combination of eye and head cues.

We have recently proposed a dual-route model of the effect of head orientation on perceived gaze direction (Otsuka, Mareschal, Calder, & Clifford, 2014; Otsuka, Mareschal, & Clifford, 2015), which computes perceived gaze direction as a linear combination of eye orientation and head orientation. By parametrically manipulating eye orientation and head orientation, we tested the adequacy of a linear model to account for the effect of horizontal head orientation on perceived direction of gaze. Here, participants adjusted an on-screen pointer toward the perceived gaze direction in two image conditions: Normal condition and Wollaston condition. Images in the Normal condition included a change in the visible part of the eye along with the change in head orientation, while images in the Wollaston condition were manipulated to have identical eye regions across head orientations. Multiple regression analysis with explanatory variables of eye orientation and head orientation revealed that linear models account for most of the variance both in the Normal condition and in the Wollaston condition. Further, we found no evidence that the model with a nonlinear term explains significantly more variance. Thus, the current study supports the dual-route model that computes the perceived gaze direction as a linear combination of eye orientation and head orientation.

Wollaston's effect in infants: Do infants integrate eye and head information in gaze perception?

The current study examined infants' sensitivity to Wollaston's effect: When identical eyes are placed in differently angled faces, the perceived gaze direction shifts toward the orientation of the face such that physically, the direct gaze is perceived as averted toward the orientation of the face. Consistent with Wollaston's effect, we found that looking toward direct and averted gaze by 4- to 5- and 7- to 8-month-olds (n = 40) was affected by the head orientation context. These results demonstrate that infants aged 4 to 5 and 7 to 8 months integrate eye and head information to perceive another's gaze direction. In light of recent psychophysical findings, the current results suggest that the visual function supporting constant gaze perception across head rotation is already at work by 4 to 5 months of age.

Orientation decoding: Sense in spirals?

The orientation of a visual stimulus can be successfully decoded from the multivariate pattern of fMRI activity in human visual cortex. Whether this capacity requires coarse-scale orientation biases is controversial. We and others have advocated the use of spiral stimuli to eliminate a potential coarse-scale bias-the radial bias toward local orientations that are collinear with the centre of gaze-and hence narrow down the potential coarse-scale biases that could contribute to orientation decoding. The usefulness of this strategy is challenged by the computational simulations of Carlson (2014), who reported the ability to successfully decode spirals of opposite sense (opening clockwise or counter-clockwise) from the pooled output of purportedly unbiased orientation filters. Here, we elaborate the mathematical relationship between spirals of opposite sense to confirm that they cannot be discriminated on the basis of the pooled output of unbiased or radially biased orientation filters. We then demonstrate that Carlson's (2014) reported decoding ability is consistent with the presence of inadvertent biases in the set of orientation filters; biases introduced by their digital implementation and unrelated to the brain's processing of orientation. These analyses demonstrate that spirals must be processed with an orientation bias other than the radial bias for successful decoding of spiral sense.

Orientation anisotropies in human primary visual cortex depend on contrast.

Orientation processing in visual cortex appears matched to the environment, such that larger neural populations are tuned to cardinal (horizontal/vertical) than oblique orientations. This may be manifested perceptually as a cardinal bias: poorer sensitivity to oblique compared to cardinal orientations (the "oblique effect"). However, a growing body of psychophysical data reveals the opposite pattern of anisotropy: a bias towards the oblique over the cardinal orientations (the "horizontal effect"), something matched by recent functional magnetic resonance imaging (fMRI) studies that have found an increased response to the oblique over the cardinal orientations in early visual cortex. This may reveal the operation of an efficient coding strategy optimised to the diet of orientations encountered during natural viewing. From consideration of coding efficiency, it might be expected that the anisotropies would change as the quality/strength of the oriented stimulus changes. In two experiments, fMRI response modulations were measured in retinotopically-defined human early visual cortex as a function of the contrast and orientation of sinusoidal gratings. Both experiments revealed a marked change in the V1 response from a cardinal (vertical) bias at low contrast to an oblique bias at high contrast. In Experiment 2, this was also apparent in areas V2 and V3. On average, there was no systematic "radial bias" (a preference for orientations aligned with the visual field meridian) in V1, although it was present in some individual subjects. The change in orientation anisotropies with contrast is consistent with an adaptive stimulus coding strategy in cortex that shifts according to the strength of the sensory inputs.

Population decoding in rat barrel cortex: optimizing the linear readout of correlated population responses.

Sensory information is encoded in the response of neuronal populations. How might this information be decoded by downstream neurons? Here we analyzed the responses of simultaneously recorded barrel cortex neurons to sinusoidal vibrations of varying amplitudes preceded by three adapting stimuli of 0, 6 and 12 µm in amplitude. Using the framework of signal detection theory, we quantified the performance of a linear decoder which sums the responses of neurons after applying an optimum set of weights. Optimum weights were found by the analytical solution that maximized the average signal-to-noise ratio based on Fisher linear discriminant analysis. This provided a biologically plausible decoder that took into account the neuronal variability, covariability, and signal correlations. The optimal decoder achieved consistent improvement in discrimination performance over simple pooling. Decorrelating neuronal responses by trial shuffling revealed that, unlike pooling, the performance of the optimal decoder was minimally affected by noise correlation. In the non-adapted state, noise correlation enhanced the performance of the optimal decoder for some populations. Under adaptation, however, noise correlation always degraded the performance of the optimal decoder. Nonetheless, sensory adaptation improved the performance of the optimal decoder mainly by increasing signal correlation more than noise correlation. Adaptation induced little systematic change in the relative direction of signal and noise. Thus, a decoder which was optimized under the non-adapted state generalized well across states of adaptation.