The visible gorilla: Unexpected fast-not physically salient-Objects are noticeable.

It is widely believed that observers can fail to notice clearly visible unattended objects, even if they are moving. Here, we created parametric tasks to test this belief and report the results of three high-powered experiments (total n = 4,493) indicating that this effect is strongly modulated by the speed of the unattended object. Specifically, fast-but not slow-objects are readily noticeable, whether they are attended or not. These results suggest that fast motion serves as a potent exogenous cue that overrides task-focused attention, showing that fast speeds, not long exposure duration or physical salience, strongly diminish inattentional blindness effects.

An image-computable model of how endogenous and exogenous attention differentially alter visual perception.

Attention alters perception across the visual field. Typically, endogenous (voluntary) and exogenous (involuntary) attention similarly improve performance in many visual tasks, but they have differential effects in some tasks. Extant models of visual attention assume that the effects of these two types of attention are identical and consequently do not explain differences between them. Here, we develop a model of spatial resolution and attention that distinguishes between endogenous and exogenous attention. We focus on texture-based segmentation as a model system because it has revealed a clear dissociation between both attention types. For a texture for which performance peaks at parafoveal locations, endogenous attention improves performance across eccentricity, whereas exogenous attention improves performance where the resolution is low (peripheral locations) but impairs it where the resolution is high (foveal locations) for the scale of the texture. Our model emulates sensory encoding to segment figures from their background and predict behavioral performance. To explain attentional effects, endogenous and exogenous attention require separate operating regimes across visual detail (spatial frequency). Our model reproduces behavioral performance across several experiments and simultaneously resolves three unexplained phenomena: 1) the parafoveal advantage in segmentation, 2) the uniform improvements across eccentricity by endogenous attention, and 3) the peripheral improvements and foveal impairments by exogenous attention. Overall, we unveil a computational dissociation between each attention type and provide a generalizable framework for predicting their effects on perception across the visual field.

A recurrent circuit implements normalization, simulating the dynamics of V1 activity.

The normalization model has been applied to explain neural activity in diverse neural systems including primary visual cortex (V1). The model's defining characteristic is that the response of each neuron is divided by a factor that includes a weighted sum of activity of a pool of neurons. Despite the success of the normalization model, there are three unresolved issues. 1) Experimental evidence supports the hypothesis that normalization in V1 operates via recurrent amplification, i.e., amplifying weak inputs more than strong inputs. It is unknown how normalization arises from recurrent amplification. 2) Experiments have demonstrated that normalization is weighted such that each weight specifies how one neuron contributes to another's normalization pool. It is unknown how weighted normalization arises from a recurrent circuit. 3) Neural activity in V1 exhibits complex dynamics, including gamma oscillations, linked to normalization. It is unknown how these dynamics emerge from normalization. Here, a family of recurrent circuit models is reported, each of which comprises coupled neural integrators to implement normalization via recurrent amplification with arbitrary normalization weights, some of which can recapitulate key experimental observations of the dynamics of neural activity in V1.

Heading perception depends on time-varying evolution of optic flow.

There is considerable support for the hypothesis that perception of heading in the presence of rotation is mediated by instantaneous optic flow. This hypothesis, however, has never been tested. We introduce a method, termed "nonvarying phase motion," for generating a stimulus that conveys a single instantaneous optic flow field, even though the stimulus is presented for an extended period of time. In this experiment, observers viewed stimulus videos and performed a forced-choice heading discrimination task. For nonvarying phase motion, observers made large errors in heading judgments. This suggests that instantaneous optic flow is insufficient for heading perception in the presence of rotation. These errors were mostly eliminated when the velocity of phase motion was varied over time to convey the evolving sequence of optic flow fields corresponding to a particular heading. This demonstrates that heading perception in the presence of rotation relies on the time-varying evolution of optic flow. We hypothesize that the visual system accurately computes heading, despite rotation, based on optic acceleration, the temporal derivative of optic flow.

Oscillatory recurrent gated neural integrator circuits (ORGaNICs), a unifying theoretical framework for neural dynamics.

Working memory is an example of a cognitive and neural process that is not static but evolves dynamically with changing sensory inputs; another example is motor preparation and execution. We introduce a theoretical framework for neural dynamics, based on oscillatory recurrent gated neural integrator circuits (ORGaNICs), and apply it to simulate key phenomena of working memory and motor control. The model circuits simulate neural activity with complex dynamics, including sequential activity and traveling waves of activity, that manipulate (as well as maintain) information during working memory. The same circuits convert spatial patterns of premotor activity to temporal profiles of motor control activity and manipulate (e.g., time warp) the dynamics. Derivative-like recurrent connectivity, in particular, serves to manipulate and update internal models, an essential feature of working memory and motor execution. In addition, these circuits incorporate recurrent normalization, to ensure stability over time and robustness with respect to perturbations of synaptic weights.

Position-theta-phase model of hippocampal place cell activity applied to quantification of running speed modulation of firing rate.

Spiking activity of place cells in the hippocampus encodes the animal's position as it moves through an environment. Within a cell's place field, both the firing rate and the phase of spiking in the local theta oscillation contain spatial information. We propose a position-theta-phase (PTP) model that captures the simultaneous expression of the firing-rate code and theta-phase code in place cell spiking. This model parametrically characterizes place fields to compare across cells, time, and conditions; generates realistic place cell simulation data; and conceptualizes a framework for principled hypothesis testing to identify additional features of place cell activity. We use the PTP model to assess the effect of running speed in place cell data recorded from rats running on linear tracks. For the majority of place fields, we do not find evidence for speed modulation of the firing rate. For a small subset of place fields, we find firing rates significantly increase or decrease with speed. We use the PTP model to compare candidate mechanisms of speed modulation in significantly modulated fields and determine that speed acts as a gain control on the magnitude of firing rate. Our model provides a tool that connects rigorous analysis with a computational framework for understanding place cell activity.

Uncharacteristic Task-Evoked Pupillary Responses Implicate Atypical Locus Ceruleus Activity in Autism.

Autism spectrum disorder (ASD) is characterized partly by atypical attentional engagement, reflected in exaggerated and variable responses to sensory stimuli. Attentional engagement is known to be regulated by the locus ceruleus (LC). Moderate baseline LC activity globally dampens neural responsivity and is associated with adaptive deployment and narrowing of attention to task-relevant stimuli. In contrast, increased baseline LC activity enhances neural responsivity across cortex and widening of attention to environmental stimuli regardless of their task relevance. Given attentional atypicalities in ASD, this study is the first to evaluate whether, under different attentional task demands, individuals with ASD exhibit a different profile of LC activity compared with typically developing controls. Males and females with ASD and age- and gender-matched controls participated in a one-back letter detection test while task-evoked pupillary responses, an established correlate for LC activity, were recorded. Participants completed this task in two conditions, either in the absence or presence of distractor auditory tones. Compared with controls, individuals with ASD evinced atypical pupillary responses in the presence versus absence of distractors. Notably, this atypical pupillary profile was evident despite the fact that both groups exhibited equivalent task performance. Moreover, between-group differences in pupillary responses were observed specifically in response to task-relevant events, providing confirmation that the group differences most likely were specifically associated with distinctions in LC activity. These findings suggest that individuals with ASD show atypical modulation of LC activity with changes in attentional demands, offering a possible mechanistic and neurobiological account for attentional atypicalities in ASD.SIGNIFICANCE STATEMENT Individuals with autism spectrum disorder (ASD) exhibit atypical attentional behaviors, including altered sensory responses and atypical fixedness, but the neural mechanism underlying these behaviors remains elusive. One candidate mechanism is atypical locus ceruleus (LC) activity, as the LC plays a critical role in attentional modulation. Specifically, LC activity is involved in regulating the trade-off between environmental exploration and focused attention. This study shows that, under tightly controlled conditions, task-evoked pupil responses, an LC activity proxy, are lower in individuals with ASD than in controls, but only in the presence of task-irrelevant stimuli. This suggests that individuals with ASD evince atypical modulation of LC activity in accordance with changes in attentional demands, offering a mechanistic account for attentional atypicalities in ASD.

Theory of cortical function.

Most models of sensory processing in the brain have a feedforward architecture in which each stage comprises simple linear filtering operations and nonlinearities. Models of this form have been used to explain a wide range of neurophysiological and psychophysical data, and many recent successes in artificial intelligence (with deep convolutional neural nets) are based on this architecture. However, neocortex is not a feedforward architecture. This paper proposes a first step toward an alternative computational framework in which neural activity in each brain area depends on a combination of feedforward drive (bottom-up from the previous processing stage), feedback drive (top-down context from the next stage), and prior drive (expectation). The relative contributions of feedforward drive, feedback drive, and prior drive are controlled by a handful of state parameters, which I hypothesize correspond to neuromodulators and oscillatory activity. In some states, neural responses are dominated by the feedforward drive and the theory is identical to a conventional feedforward model, thereby preserving all of the desirable features of those models. In other states, the theory is a generative model that constructs a sensory representation from an abstract representation, like memory recall. In still other states, the theory combines prior expectation with sensory input, explores different possible perceptual interpretations of ambiguous sensory inputs, and predicts forward in time. The theory, therefore, offers an empirically testable framework for understanding how the cortex accomplishes inference, exploration, and prediction.

Attention model of binocular rivalry.

When the corresponding retinal locations in the two eyes are presented with incompatible images, a stable percept gives way to perceptual alternations in which the two images compete for perceptual dominance. As perceptual experience evolves dynamically under constant external inputs, binocular rivalry has been used for studying intrinsic cortical computations and for understanding how the brain regulates competing inputs. Converging behavioral and EEG results have shown that binocular rivalry and attention are intertwined: binocular rivalry ceases when attention is diverted away from the rivalry stimuli. In addition, the competing image in one eye suppresses the target in the other eye through a pattern of gain changes similar to those induced by attention. These results require a revision of the current computational theories of binocular rivalry, in which the role of attention is ignored. Here, we provide a computational model of binocular rivalry. In the model, competition between two images in rivalry is driven by both attentional modulation and mutual inhibition, which have distinct selectivity (feature vs. eye of origin) and dynamics (relatively slow vs. relatively fast). The proposed model explains a wide range of phenomena reported in rivalry, including the three hallmarks: (i) binocular rivalry requires attention; (ii) various perceptual states emerge when the two images are swapped between the eyes multiple times per second; (iii) the dominance duration as a function of input strength follows Levelt's propositions. With a bifurcation analysis, we identified the parameter space in which the model's behavior was consistent with experimental results.

Temporal Contingencies Determine Whether Adaptation Strengthens or Weakens Normalization.

A fundamental and nearly ubiquitous feature of sensory encoding is that neuronal responses are strongly influenced by recent experience, or adaptation. Theoretical and computational studies have proposed that many adaptation effects may result in part from changes in the strength of normalization signals. Normalization is a "canonical" computation in which a neuron's response is modulated (normalized) by the pooled activity of other neurons. Here, we test whether adaptation can alter the strength of cross-orientation suppression, or masking, a paradigmatic form of normalization evident in primary visual cortex (V1). We made extracellular recordings of V1 neurons in anesthetized male macaques and measured responses to plaid stimuli composed of two overlapping, orthogonal gratings before and after prolonged exposure to two distinct adapters. The first adapter was a plaid consisting of orthogonal gratings and led to stronger masking. The second adapter presented the same orthogonal gratings in an interleaved manner and led to weaker masking. The strength of adaptation's effects on masking depended on the orientation of the test stimuli relative to the orientation of the adapters, but was independent of neuronal orientation preference. Changes in masking could not be explained by altered neuronal responsivity. Our results suggest that normalization signals can be strengthened or weakened by adaptation depending on the temporal contingencies of the adapting stimuli. Our findings reveal an interplay between two widespread computations in cortical circuits, adaptation and normalization, that enables flexible adjustments to the structure of the environment, including the temporal relationships among sensory stimuli.SIGNIFICANCE STATEMENT Two fundamental features of sensory responses are that they are influenced by adaptation and that they are modulated by the activity of other nearby neurons via normalization. Our findings reveal a strong interaction between these two aspects of cortical computation. Specifically, we show that cross-orientation masking, a form of normalization, can be strengthened or weakened by adaptation depending on the temporal contingencies between sensory inputs. Our findings support theoretical proposals that some adaptation effects may involve altered normalization and offer a network-based explanation for how cortex adjusts to current sensory demands.

Specific Visual Subregions of TPJ Mediate Reorienting of Spatial Attention.

The temporo-parietal junction (TPJ) has been associated with various cognitive and social functions, and is critical for attentional reorienting. Attention affects early visual processing. Neuroimaging studies dealing with such processes have thus far concentrated on striate and extrastriate areas. Here, we investigated whether attention orienting or reorienting modulate activity in visually driven TPJ subregions. For each observer we identified 3 visually responsive subregions within TPJ: 2 bilateral (vTPJant and vTPJpost) and 1 right lateralized (vTPJcent). Cortical activity in these subregions was measured using fMRI while observers performed a 2-alternative forced-choice orientation discrimination task. Covert spatial endogenous (voluntary) or exogenous (involuntary) attention was manipulated using either a central or a peripheral cue with task, stimuli and observers constant. Both endogenous and exogenous attention increased activity for invalidly cued trials in right vTPJpost; only endogenous attention increased activity for invalidly cued trials in left vTPJpost and in right vTPJcent; and neither type of attention modulated either right or left vTPJant. These results demonstrate that vTPJpost and vTPJcent mediate the reorientation of covert attention to task relevant stimuli, thus playing a critical role in visual attention. These findings reveal a differential reorienting cortical response after observers' attention has been oriented to a given location voluntarily or involuntarily.

On spatial attention and its field size on the repulsion effect.

We investigated the attentional repulsion effect-stimuli appear displaced further away from attended locations-in three experiments: one with exogenous (involuntary) attention, and two with endogenous (voluntary) attention with different attention-field sizes. It has been proposed that differences in attention-field size can account for qualitative differences in neural responses elicited by attended stimuli. We used psychophysical comparative judgments and manipulated either exogenous attention via peripheral cues or endogenous attention via central cues and a demanding rapid serial visual presentation task. We manipulated the attention field size of endogenous attention by presenting streams of letters at two specific locations or at two of many possible locations during each block. We found a robust attentional repulsion effect in all three experiments: with endogenous and exogenous attention and with both attention-field sizes. These findings advance our understanding of the influence of spatial attention on the perception of visual space and help relate this repulsion effect to possible neurophysiological correlates.

Pattern Adaptation and Normalization Reweighting.

UNLABELLED: Adaptation to an oriented stimulus changes both the gain and preferred orientation of neural responses in V1. Neurons tuned near the adapted orientation are suppressed, and their preferred orientations shift away from the adapter. We propose a model in which weights of divisive normalization are dynamically adjusted to homeostatically maintain response products between pairs of neurons. We demonstrate that this adjustment can be performed by a very simple learning rule. Simulations of this model closely match existing data from visual adaptation experiments. We consider several alternative models, including variants based on homeostatic maintenance of response correlations or covariance, as well as feedforward gain-control models with multiple layers, and we demonstrate that homeostatic maintenance of response products provides the best account of the physiological data. SIGNIFICANCE STATEMENT: Adaptation is a phenomenon throughout the nervous system in which neural tuning properties change in response to changes in environmental statistics. We developed a model of adaptation that combines normalization (in which a neuron's gain is reduced by the summed responses of its neighbors) and Hebbian learning (in which synaptic strength, in this case divisive normalization, is increased by correlated firing). The model is shown to account for several properties of adaptation in primary visual cortex in response to changes in the statistics of contour orientation.

Normalization as a canonical neural computation.

There is increasing evidence that the brain relies on a set of canonical neural computations, repeating them across brain regions and modalities to apply similar operations to different problems. A promising candidate for such a computation is normalization, in which the responses of neurons are divided by a common factor that typically includes the summed activity of a pool of neurons. Normalization was developed to explain responses in the primary visual cortex and is now thought to operate throughout the visual system, and in many other sensory modalities and brain regions. Normalization may underlie operations such as the representation of odours, the modulatory effects of visual attention, the encoding of value and the integration of multisensory information. Its presence in such a diversity of neural systems in multiple species, from invertebrates to mammals, suggests that it serves as a canonical neural computation.

Deconstructing Interocular Suppression: Attention and Divisive Normalization.

In interocular suppression, a suprathreshold monocular target can be rendered invisible by a salient competitor stimulus presented in the other eye. Despite decades of research on interocular suppression and related phenomena (e.g., binocular rivalry, flash suppression, continuous flash suppression), the neural processing underlying interocular suppression is still unknown. We developed and tested a computational model of interocular suppression. The model included two processes that contributed to the strength of interocular suppression: divisive normalization and attentional modulation. According to the model, the salient competitor induced a stimulus-driven attentional modulation selective for the location and orientation of the competitor, thereby increasing the gain of neural responses to the competitor and reducing the gain of neural responses to the target. Additional suppression was induced by divisive normalization in the model, similar to other forms of visual masking. To test the model, we conducted psychophysics experiments in which both the size and the eye-of-origin of the competitor were manipulated. For small and medium competitors, behavioral performance was consonant with a change in the response gain of neurons that responded to the target. But large competitors induced a contrast-gain change, even when the competitor was split between the two eyes. The model correctly predicted these results and outperformed an alternative model in which the attentional modulation was eye specific. We conclude that both stimulus-driven attention (selective for location and feature) and divisive normalization contribute to interocular suppression.

Spontaneous microsaccades reflect shifts in covert attention.

Microsaccade rate during fixation is modulated by the presentation of a visual stimulus. When the stimulus is an endogenous attention cue, the ensuing microsaccades tend to be directed toward the cue. This finding has been taken as evidence that microsaccades index the locus of spatial attention. But the vast majority of microsaccades that subjects make are not triggered by visual stimuli. Under natural viewing conditions, spontaneous microsaccades occur frequently (2-3 Hz), even in the absence of a stimulus or a task. While spontaneous microsaccades may depend on low-level visual demands, such as retinal fatigue, image fading, or fixation shifts, it is unknown whether their occurrence corresponds to changes in the attentional state. We developed a protocol to measure whether spontaneous microsaccades reflect shifts in spatial attention. Human subjects fixated a cross while microsaccades were detected from streaming eye-position data. Detection of a microsaccade triggered the appearance of a peripheral ring of grating patches, which were followed by an arrow (a postcue) indicating one of them as the target. The target was either congruent or incongruent (opposite) with respect to the direction of the microsaccade (which preceded the stimulus). Subjects reported the tilt of the target (clockwise or counterclockwise relative to vertical). We found that accuracy was higher for congruent than for incongruent trials. We conclude that the direction of spontaneous microsaccades is inherently linked to shifts in spatial attention.

Motion direction biases and decoding in human visual cortex.

Functional magnetic resonance imaging (fMRI) studies have relied on multivariate analysis methods to decode visual motion direction from measurements of cortical activity. Above-chance decoding has been commonly used to infer the motion-selective response properties of the underlying neural populations. Moreover, patterns of reliable response biases across voxels that underlie decoding have been interpreted to reflect maps of functional architecture. Using fMRI, we identified a direction-selective response bias in human visual cortex that: (1) predicted motion-decoding accuracy; (2) depended on the shape of the stimulus aperture rather than the absolute direction of motion, such that response amplitudes gradually decreased with distance from the stimulus aperture edge corresponding to motion origin; and 3) was present in V1, V2, V3, but not evident in MT+, explaining the higher motion-decoding accuracies reported previously in early visual cortex. These results demonstrate that fMRI-based motion decoding has little or no dependence on the underlying functional organization of motion selectivity.

Long-range traveling waves of activity triggered by local dichoptic stimulation in V1 of behaving monkeys.

Traveling waves of cortical activity, in which local stimulation triggers lateral spread of activity to distal locations, have been hypothesized to play an important role in cortical function. However, there is conflicting physiological evidence for the existence of spreading traveling waves of neural activity triggered locally. Dichoptic stimulation, in which the two eyes view dissimilar monocular patterns, can lead to dynamic wave-like fluctuations in visual perception and therefore, provides a promising means for identifying and studying cortical traveling waves. Here, we used voltage-sensitive dye imaging to test for the existence of traveling waves of activity in the primary visual cortex of awake, fixating monkeys viewing dichoptic stimuli. We find clear traveling waves that are initiated by brief, localized contrast increments in one of the monocular patterns and then, propagate at speeds of ∼ 30 mm/s. These results demonstrate that under an appropriate visual context, circuitry in visual cortex in alert animals is capable of supporting long-range traveling waves triggered by local stimulation.

Normalization in human somatosensory cortex.

Functional magnetic resonance imaging (fMRI) was used to measure activity in human somatosensory cortex and to test for cross-digit suppression. Subjects received stimulation (vibration of varying amplitudes) to the right thumb (target) with or without concurrent stimulation of the right middle finger (mask). Subjects were less sensitive to target stimulation (psychophysical detection thresholds were higher) when target and mask digits were stimulated concurrently compared with when the target was stimulated in isolation. fMRI voxels in a region of the left postcentral gyrus each responded when either digit was stimulated. A regression model (called a forward model) was used to separate the fMRI measurements from these voxels into two hypothetical channels, each of which responded selectively to only one of the two digits. For the channel tuned to the target digit, responses in the left postcentral gyrus increased with target stimulus amplitude but were suppressed by concurrent stimulation to the mask digit, evident as a shift in the gain of the response functions. For the channel tuned to the mask digit, a constant baseline response was evoked for all target amplitudes when the mask was absent and responses decreased with increasing target amplitude when the mask was concurrently presented. A computational model based on divisive normalization provided a good fit to the measurements for both mask-absent and target + mask stimulation. We conclude that the normalization model can explain cross-digit suppression in human somatosensory cortex, supporting the hypothesis that normalization is a canonical neural computation.

Continuous flash suppression modulates cortical activity in early visual cortex.

A salient visual stimulus can be rendered invisible by presenting it to one eye while flashing a mask to the other eye. This procedure, called continuous flash suppression (CFS), has been proposed as an ideal way of studying awareness as it can make a stimulus imperceptible for extended periods of time. Previous studies have reported robust suppression of cortical activity in higher visual areas during CFS, but the role of primary visual cortex (V1) is still controversial. In this study, we resolve this controversy on the role of V1 in CFS and also begin characterizing the computational processes underlying CFS. Early visual cortical activity was measured with functional magnetic resonance imaging while human subjects viewed stimuli composed of target and mask, presented to the same or different eyes. Functional MRI responses in early visual cortex were smaller when target and mask were in different eyes compared with the same eye, not only for the lowest contrast target rendered invisible by CFS, but also for higher contrast targets, which were visible even when presented to the eye opposite the mask. We infer that CFS is based on modulating the gain of neural responses, akin to reducing target contrast.