Distinct Patterns of Connectivity between Brain Regions Underlie the Intra-Modal and Cross-Modal Value-Driven Modulations of the Visual Cortex.

Past reward associations may be signaled from different sensory modalities; however, it remains unclear how different types of reward-associated stimuli modulate sensory perception. In this human fMRI study (female and male participants), a visual target was simultaneously presented with either an intra- (visual) or a cross-modal (auditory) cue that was previously associated with rewards. We hypothesized that, depending on the sensory modality of the cues, distinct neural mechanisms underlie the value-driven modulation of visual processing. Using a multivariate approach, we confirmed that reward-associated cues enhanced the target representation in early visual areas and identified the brain valuation regions. Then, using an effective connectivity analysis, we tested three possible patterns of connectivity that could underlie the modulation of the visual cortex: a direct pathway from the frontal valuation areas to the visual areas, a mediated pathway through the attention-related areas, and a mediated pathway that additionally involved sensory association areas. We found evidence for the third model demonstrating that the reward-related information in both sensory modalities is communicated across the valuation and attention-related brain regions. Additionally, the superior temporal areas were recruited when reward was cued cross-modally. The strongest dissociation between the intra- and cross-modal reward-driven effects was observed at the level of the feedforward and feedback connections of the visual cortex estimated from the winning model. These results suggest that, in the presence of previously rewarded stimuli from different sensory modalities, a combination of domain-general and domain-specific mechanisms are recruited across the brain to adjust the visual perception.SIGNIFICANCE STATEMENT Reward has a profound effect on perception, but it is not known whether shared or disparate mechanisms underlie the reward-driven effects across sensory modalities. In this human fMRI study, we examined the reward-driven modulation of the visual cortex by visual (intra-modal) and auditory (cross-modal) reward-associated cues. Using a model-based approach to identify the most plausible pattern of inter-regional effective connectivity, we found that higher-order areas involved in the valuation and attentional processing were recruited by both types of rewards. However, the pattern of connectivity between these areas and the early visual cortex was distinct between the intra- and cross-modal rewards. This evidence suggests that, to effectively adapt to the environment, reward signals may recruit both domain-general and domain-specific mechanisms.

The effect of subliminal incentives on goal-directed eye movements.

Over the last decades, several studies have demonstrated that conscious and unconscious reward incentives both affect performance in physical and cognitive tasks, suggesting that goal pursuit can arise from an unconscious will. Whether the planning of goal-directed saccadic eye movements during an effortful task can also be affected by subliminal reward cues has not been systematically investigated. We employed a novel task where participants made several eye movements back and forth between a fixation point and a number of peripheral targets. The total number of targets visited by the eyes in a fixed amount of time determined participants' monetary gain. The magnitude of the reward at stake was briefly shown at the beginning of each trial and masked by pattern images superimposed in time so that at shorter display durations participants perceived reward incentives subliminally. We found a main effect of reward across all display durations as higher reward enhanced participants' oculomotor effort measured as the frequency and peak velocity of saccades. This effect was strongest for consciously perceived rewards but also occurred when rewards were subliminally perceived. Although we did not find a statistically significant dissociation between the reward-related modulation of different saccadic parameters, across two experiments the most robust effect of subliminal rewards was observed for the modulation of the saccadic frequency but not the peak velocity. These results suggest that multiple indices of oculomotor effort can be incentivized by subliminal rewards and that saccadic frequency may provide the most sensitive indicator of subliminal incentivization of eye movements. NEW & NOTEWORTHY Reward incentives motivate humans to exert more effort, and they do so even when rewards are subconsciously perceived. It has been unknown whether these effects also extend to eye movements that have lower energetic demands compared with other movement types. We devised a behavioral task that required fast execution of multiple eye movements. Subliminal rewards enhanced the frequency and peak velocity of saccadic eye movements, with the most reliable effect observed for saccadic frequency.

Receipt of reward leads to altered estimation of effort.

Effort and reward jointly shape many human decisions. Errors in predicting the required effort needed for a task can lead to suboptimal behavior. Here, we show that effort estimations can be biased when retrospectively reestimated following receipt of a rewarding outcome. These biases depend on the contingency between reward and task difficulty and are stronger for highly contingent rewards. Strikingly, the observed pattern accords with predictions from Bayesian cue integration, indicating humans deploy an adaptive and rational strategy to deal with inconsistencies between the efforts they expend and the ensuing rewards.

Learning a New Selection Rule in Visual and Frontal Cortex.

How do you make a decision if you do not know the rules of the game? Models of sensory decision-making suggest that choices are slow if evidence is weak, but they may only apply if the subject knows the task rules. Here, we asked how the learning of a new rule influences neuronal activity in the visual (area V1) and frontal cortex (area FEF) of monkeys. We devised a new icon-selection task. On each day, the monkeys saw 2 new icons (small pictures) and learned which one was relevant. We rewarded eye movements to a saccade target connected to the relevant icon with a curve. Neurons in visual and frontal cortex coded the monkey's choice, because the representation of the selected curve was enhanced. Learning delayed the neuronal selection signals and we uncovered the cause of this delay in V1, where learning to select the relevant icon caused an early suppression of surrounding image elements. These results demonstrate that the learning of a new rule causes a transition from fast and random decisions to a more considerate strategy that takes additional time and they reveal the contribution of visual and frontal cortex to the learning process.

Simultaneous selection by object-based attention in visual and frontal cortex.

Models of visual attention hold that top-down signals from frontal cortex influence information processing in visual cortex. It is unknown whether situations exist in which visual cortex actively participates in attentional selection. To investigate this question, we simultaneously recorded neuronal activity in the frontal eye fields (FEF) and primary visual cortex (V1) during a curve-tracing task in which attention shifts are object-based. We found that accurate performance was associated with similar latencies of attentional selection in both areas and that the latency in both areas increased if the task was made more difficult. The amplitude of the attentional signals in V1 saturated early during a trial, whereas these selection signals kept increasing for a longer time in FEF, until the moment of an eye movement, as if FEF integrated attentional signals present in early visual cortex. In erroneous trials, we observed an interareal latency difference because FEF selected the wrong curve before V1 and imposed its erroneous decision onto visual cortex. The neuronal activity in visual and frontal cortices was correlated across trials, and this trial-to-trial coupling was strongest for the attended curve. These results imply that selective attention relies on reciprocal interactions within a large network of areas that includes V1 and FEF.

Cross-modal effects of value on perceptual acuity and stimulus encoding.

Cross-modal interactions are very common in perception. An important feature of many perceptual stimuli is their reward-predicting properties, the utilization of which is essential for adaptive behavior. What is unknown is whether reward associations in one sensory modality influence perception of stimuli in another modality. Here we show that auditory stimuli with high-reward associations increase the sensitivity of visual perception, even when sounds and reward associations are both irrelevant for the visual task. This increased sensitivity correlates with a change in stimulus representation in the visual cortex, indexed by increased multivariate decoding accuracy in simultaneously acquired functional MRI data. Univariate analysis showed that reward associations modulated responses in regions associated with multisensory processing in which the strength of modulation was a better predictor of the magnitude of the behavioral effect than the modulation in classical reward regions. Our findings demonstrate a value-driven cross-modal interaction that affects perception and stimulus encoding, with a resemblance to well-described modulatory effects of attention. We suggest that multisensory processing areas may mediate the transfer of value signals across senses.

Blood oxygen level-dependent activation of the primary visual cortex predicts size adaptation illusion.

In natural scenes, objects rarely occur in isolation but appear within a spatiotemporal context. Here, we show that the perceived size of a stimulus is significantly affected by the context of the scene: brief previous presentation of larger or smaller adapting stimuli at the same region of space changes the perceived size of a test stimulus, with larger adapting stimuli causing the test to appear smaller than veridical and vice versa. In a human fMRI study, we measured the blood oxygen level-dependent activation (BOLD) responses of the primary visual cortex (V1) to the contours of large-diameter stimuli and found that activation closely matched the perceptual rather than the retinal stimulus size: the activated area of V1 increased or decreased, depending on the size of the preceding stimulus. A model based on local inhibitory V1 mechanisms simulated the inward or outward shifts of the stimulus contours and hence the perceptual effects. Our findings suggest that area V1 is actively involved in reshaping our perception to match the short-term statistics of the visual scene.

The effect of visual salience on memory-based choices.

Deciding whether a stimulus is the "same" or "different" from a previous presented one involves integrating among the incoming sensory information, working memory, and perceptual decision making. Visual selective attention plays a crucial role in selecting the relevant information that informs a subsequent course of action. Previous studies have mainly investigated the role of visual attention during the encoding phase of working memory tasks. In this study, we investigate whether manipulation of bottom-up attention by changing stimulus visual salience impacts on later stages of memory-based decisions. In two experiments, we asked subjects to identify whether a stimulus had either the same or a different feature to that of a memorized sample. We manipulated visual salience of the test stimuli by varying a task-irrelevant feature contrast. Subjects chose a visually salient item more often when they looked for matching features and less often so when they looked for a nonmatch. This pattern of results indicates that salient items are more likely to be identified as a match. We interpret the findings in terms of capacity limitations at a comparison stage where a visually salient item is more likely to exhaust resources leading it to be prematurely parsed as a match.

The contribution of sensory information asymmetry and bias of attribution to egocentric tendencies in effort comparison tasks.

When comparing themselves with others, people often evaluate their own behaviors more favorably. This egocentric tendency is often categorized as a bias of attribution, with favorable self-evaluation resulting from differing explanations of one's own behavior and that of others. However, studies on information availability in social contexts offer an alternative explanation, ascribing egocentric biases to the inherent informational asymmetries between performing an action and merely observing it. Since biases of attribution and availability often co-exist and interact with each other, it is not known whether they are both necessary for the egocentric biases to emerge. In this study, we used a design that allowed us to directly compare the contribution of these two distinct sources of bias to judgements about the difficulty of an effortful task. Participants exhibited no attribution bias as judgements made for themselves did not differ from those made for others. Importantly, however, participants perceived the tasks they actively performed to be harder than the tasks they observed, and this bias was magnified as the overall task difficulty increased. These findings suggest that information asymmetries inherent to the difference between actively performing a task and observing it can drive egocentric biases in effort evaluations on their own and without a contribution from biases of attribution.

Learned value modulates the access to visual awareness during continuous flash suppression.

Monetary value enhances visual perception and attention and boosts activity in the primary visual cortex, however, it is still unclear whether monetary value can modulate the conscious access to rewarding stimuli. Here we investigate this issue by employing a breaking continuous flash suppression (b-CFS) paradigm. We measured suppression durations of sinusoidal gratings having orthogonal orientations under CFS in adult volunteers before and after a short session of Pavlovian associative learning in which each orientation was arbitrarily associated either with high or low monetary reward. We found that monetary value accelerated the access to visual awareness during CFS. Specifically, after the associative learning, suppression durations of the visual stimulus associated with high monetary value were shorter compared to the visual stimulus associated with low monetary value. Critically, the effect was replicated in a second experiment using a detection task for b-CFS that was orthogonal to the reward associative learning. These results indicate that monetary reward facilitates the access to awareness of visual stimuli associated with monetary value probably by boosting their representation at the early stages of visual processing in the brain.

Differential effects of intra-modal and cross-modal reward value on perception: ERP evidence.

In natural environments objects comprise multiple features from the same or different sensory modalities but it is not known how perception of an object is affected by the value associations of its constituent parts. The present study compares intra- and cross-modal value-driven effects on behavioral and electrophysiological correlates of perception. Human participants first learned the reward associations of visual and auditory cues. Subsequently, they performed a visual discrimination task in the presence of previously rewarded, task-irrelevant visual or auditory cues (intra- and cross-modal cues, respectively). During the conditioning phase, when reward associations were learned and reward cues were the target of the task, high value stimuli of both modalities enhanced the electrophysiological correlates of sensory processing in posterior electrodes. During the post-conditioning phase, when reward delivery was halted and previously rewarded stimuli were task-irrelevant, cross-modal value significantly enhanced the behavioral measures of visual sensitivity, whereas intra-modal value produced only an insignificant decrement. Analysis of the simultaneously recorded event-related potentials (ERPs) of posterior electrodes revealed similar findings. We found an early (90-120 ms) suppression of ERPs evoked by high-value, intra-modal stimuli. Cross-modal stimuli led to a later value-driven modulation, with an enhancement of response positivity for high- compared to low-value stimuli starting at the N1 window (180-250 ms) and extending to the P3 (300-600 ms) responses. These results indicate that sensory processing of a compound stimulus comprising a visual target and task-irrelevant visual or auditory cues is modulated by the reward value of both sensory modalities, but such modulations rely on distinct underlying mechanisms.

"Non-retinotopic processing" in Ternus motion displays modeled by spatiotemporal filters.

Recently, M. Boi, H. Ogmen, J. Krummenacher, T. U. Otto, & M. H. Herzog (2009) reported a fascinating visual effect, where the direction of apparent motion was disambiguated by cues along the path of apparent motion, the Ternus-Pikler group motion, even though no actual movement occurs in this stimulus. They referred to their study as a "litmus test" to distinguish "non-retinotopic" (motion-based) from "retinotopic" (retina-based) image processing. We adapted the test to one with simple grating stimuli that could be more readily modeled and replicated their psychophysical results quantitatively with this stimulus. We then modeled our experiments in 3D (x, y, t) Fourier space and demonstrated that the observed perceptual effects are readily accounted for by integration of information within a detector that is oriented in space and time, in a similar way to previous explanations of other motion illusions. This demonstration brings the study of Boi et al. into the more general context of perception of moving objects.

Visual competition attenuates emotion effects during overt attention shifts.

Numerous different objects are simultaneously visible in a person's visual field, competing for attention. This competition has been shown to affect eye-movements and early neural responses toward stimuli, while the role of a stimulus' emotional meaning for mechanisms of overt attention shifts under competition is unclear. The current study combined EEG and eye-tracking to investigate effects of competition and emotional content on overt shifts of attention to human face stimuli. Competition prolonged the latency of the P1 component and of saccades, while faces showing emotional expressions elicited an early posterior negativity (EPN). Remarkably, the emotion-related modulation of the EPN was attenuated when two stimuli were competing for attention compared to non-competition. In contrast, no interaction effects of emotional expression and competition were observed on other event-related potentials. This finding indicates that competition can decelerate attention shifts in general and also diminish the emotion-driven attention capture, measured through the smaller effects of emotional expression on EPN amplitude. Reduction of the brain's responsiveness to emotional content in the presence of distractors contradicts models that postulate fully automatic processing of emotions.

Value-driven modulation of visual perception by visual and auditory reward cues: The role of performance-contingent delivery of reward.

Perception is modulated by reward value, an effect elicited not only by stimuli that are predictive of performance-contingent delivery of reward (PC) but also by stimuli that were previously rewarded (PR). PC and PR cues may engage different mechanisms relying on goal-driven versus stimulus-driven prioritization of high value stimuli, respectively. However, these two modes of reward modulation have not been systematically compared against each other. This study employed a behavioral paradigm where participants' visual orientation discrimination was tested in the presence of task-irrelevant visual or auditory reward cues. In the first phase (PC), correct performance led to a high or low monetary reward dependent on the identity of visual or auditory cues. In the subsequent phase (PR), visual or auditory cues were not followed by reward delivery anymore. We hypothesized that PC cues have a stronger modulatory effect on visual discrimination and pupil responses compared to PR cues. We found an overall larger task-evoked pupil dilation in PC compared to PR phase. Whereas PC and PR cues both increased the accuracy of visual discrimination, value-driven acceleration of reaction times (RTs) and pupillary responses only occurred for PC cues. The modulation of pupil size by high reward PC cues was strongly correlated with the modulation of a combined measure of speed and accuracy. These results indicate that although value-driven modulation of perception can occur even when reward delivery is halted, stronger goal-driven control elicited by PC reward cues additionally results in a more efficient balance between accuracy and speed of perceptual choices.

Separable codes for attention and luminance contrast in the primary visual cortex.

The visual system encodes the features of visual stimuli as well as their behavioral relevance. Stimuli with a high luminance contrast evoke more activity in the visual cortex than stimuli with a low contrast. At the same time, attended stimuli evoke more activity than nonattended stimuli. There is a debate about how visual features and attention jointly determine neuronal activity in the visual cortex. Some studies suggested that attention increases apparent contrast (Reynolds et al., 2000), others that attention amplifies responses by a constant factor (Williford and Maunsell, 2006), and yet others that attention and contrast have largely additive effects (Buracas and Boynton, 2007; Thiele et al., 2009). The influence of attention on contrast sensitivity differs between neurons, raising the possibility that attention and contrast could be coded conjointly in a population of neurons. Here we investigate this possibility by recording neuronal activity at multiple sites in the primary visual cortex of macaque monkeys using multielectrode recording techniques and support vector machines to decode attended stimuli as well as stimulus contrast. We find that many, but not all, V1 neurons are influenced by attention and that the effects of attention and contrast are additive on average. Stimulus contrast can be decoded from neuronal responses not strongly modulated by attention, whereas the attended stimulus can be decoded as the difference in activity of cells that are influenced by attention and cells that are not. The success of the approach suggests that visual attention and stimulus contrast are represented by largely separable codes.

Suppressive lateral interactions at parafoveal representations in primary visual cortex.

The perceptual salience and visibility of image elements is influenced by other elements in their vicinity. The perceptual effect of image elements on an adjacent target element depends on their relative orientation. Collinear flanking elements usually improve sensitivity for the target element, whereas orthogonal elements have a weaker effect. It is believed that the collinear flankers exert these effects through lateral interactions between neurons in the primary visual cortex (area V1), but the precise mechanisms underlying these contextual interactions remain unknown. Here, we directly examined this question by recording the effects of flankers on the responses of V1 neurons at parafoveal representations while monkeys performed a fixation task or a contrast detection task. We found, unexpectedly, that collinear flankers reduce the monkeys' perceptual sensitivity for a central target element. This behavioral effect was explained by a flanker-induced increase in the activity of V1 neurons in the absence of the central target stimulus, which reduced the amplitude of the target response. Our results indicate that the dominant effect of collinear flankers in parafoveal vision is suppression and suggest that these suppressive effects are caused by a decrease in the dynamic range of neurons coding the central target.

Pre-saccadic attention spreads to stimuli forming a perceptual group with the saccade target.

The pre-saccadic attention shift-a rapid increase in visual sensitivity at the target-is an inevitable precursor of saccadic eye movements. Saccade targets are often parts of the objects that are of interest to the active observer. Although the link between saccades and covert attention shifts is well established, it remains unclear if pre-saccadic attention selects the location of the eye movement target or rather the entire object that occupies this location. Indeed, several neurophysiological studies suggest that attentional modulations of neural activity in visual cortex spreads across parts of objects (e.g., elements grouped by Gestalt principles) that contain the target location of a saccade. To understand the nature of pre-saccadic attentional selection, we examined how visual sensitivity, measured in a challenging orientation discrimination task, changes during saccade preparation at locations that are perceptually grouped with the saccade target. In Experiment 1, using grouping by color in a delayed-saccade task, we found no consistent spread of attention to locations that formed a perceptual group with the saccade target. However, performance depended on the side of the stimulus arrangement relative to the saccade target location, an effect we discuss with respect to attentional momentum. In Experiment 2, employing stronger perceptual grouping cues (color and motion) and an immediate-saccade task, we obtained a reliable grouping effect: Attention spread to locations that were perceptually grouped with the saccade target while saccade preparation was underway. We also replicated the side effect observed in Experiment 1. These results provide evidence that the pre-saccadic attention spreads beyond the target location along the saccade direction, and selects scene elements that-based on Gestalt criteria-are likely to belong to the same object as the saccade target.

Overt and covert attention shifts to emotional faces: Combining EEG, eye tracking, and a go/no-go paradigm.

In everyday life, faces with emotional expressions quickly attract attention and eye movements. To study the neural mechanisms of such emotion-driven attention by means of event-related brain potentials (ERPs), tasks that employ covert shifts of attention are commonly used, in which participants need to inhibit natural eye movements towards stimuli. It remains, however, unclear how shifts of attention to emotional faces with and without eye movements differ from each other. The current preregistered study aimed to investigate neural differences between covert and overt emotion-driven attention. We combined eye tracking with measurements of ERPs to compare shifts of attention to faces with happy, angry, or neutral expressions when eye movements were either executed (go conditions) or withheld (no-go conditions). Happy and angry faces led to larger EPN amplitudes, shorter latencies of the P1 component, and faster saccades, suggesting that emotional expressions significantly affected shifts of attention. Several ERPs (N170, EPN, LPC) were augmented in amplitude when attention was shifted with an eye movement, indicating an enhanced neural processing of faces if eye movements had to be executed together with a reallocation of attention. However, the modulation of ERPs by facial expressions did not differ between the go and no-go conditions, suggesting that emotional content enhances both covert and overt shifts of attention. In summary, our results indicate that overt and covert attention shifts differ but are comparably affected by emotional content.

Previous Motor Actions Outweigh Sensory Information in Sensorimotor Statistical Learning.

Humans can use their previous experience in form of statistical priors to improve decisions. It is, however, unclear how such priors are learned and represented. Importantly, it has remained elusive whether prior learning is independent of the sensorimotor system involved in the learning process or not, as both modality-specific and modality-general learning have been reported in the past. Here, we used a saccadic eye movement task to probe the learning and representation of a spatial prior across a few trials. In this task, learning occurs in an unsupervised manner and through encountering trial-by-trial visual hints drawn from a distribution centered on the target location. Using a model-comparison approach, we found that participants' prior knowledge is largely represented in the form of their previous motor actions, with minimal influence from the previously seen visual hints. By using two different motor contexts for response (looking either at the estimated target location, or exactly opposite to it), we could further compare whether prior experience obtained in one motor context can be transferred to the other. Although learning curves were highly similar, and participants seemed to use the same strategy for both response types, they could not fully transfer their knowledge between contexts, as performance and confidence ratings dropped after a switch of the required response. Together, our results suggest that humans preferably use the internal representations of their previous motor actions, rather than past incoming sensory information, to form statistical sensorimotor priors on the timescale of a few trials.

Additive effects of attention and stimulus contrast in primary visual cortex.

Previous studies have proposed a variety of mechanisms by which attention influences neuronal activity. Here we investigated the mechanisms of attention in the striate cortex of monkeys performing a spatial or an object-based attention task at various stimulus contrasts and compared neuronal contrast response functions with and without attention. Our data are best described by an "additive" interaction: The influence of attention on the neuronal response is relatively independent of the stimulus contrast, at least when the stimulus has enough contrast to become visible. This shows that attention adds to the neuronal responses in a largely contrast invariant manner. These data support recent functional magnetic resonance imaging studies and suggest that feedback from higher areas exerts a constant attentional drive that is mostly task not stimulus driven.