Objects that promise rewards are prioritized for visual selection. The way this prioritization shapes sensory processing in visual cortex, however, is debated. It has been suggested that rewards motivate stronger attentional focusing, resulting in a modulation of sensory selection in early visual cortex. An open question is whether those reward-driven modulations would be independent of similar modulations indexing the selection of attended features that are not associated with reward. Here, we use magnetoencephalography in human observers to investigate whether the modulations indexing global color-based selection in visual cortex are separable for target- and (monetary) reward-defining colors. To assess the underlying global color-based activity modulation, we compare the event-related magnetic field response elicited by a color probe in the unattended hemifield drawn either in the target color, the reward color, both colors, or a neutral task-irrelevant color. To test whether target and reward relevance trigger separable modulations, we manipulate attention demands on target selection while keeping reward-defining experimental parameters constant. Replicating previous observations, we find that reward and target relevance produce almost indistinguishable gain modulations in ventral extratriate cortex contralateral to the unattended color probe. Importantly, increasing attention demands on target discrimination increases the response to the target-defining color, whereas the response to the rewarded color remains largely unchanged. These observations indicate that, although task relevance and reward influence the very same feature-selective area in extrastriate visual cortex, the associated modulations are largely independent.

When a stimulus is associated with a reward, it becomes prioritized, and the allocation of attention to that stimulus increases. For low-level features, such as color, this reward-based allocation of attention can manifest early in time and as a faster and stronger shift of attention to targets with that color, as reflected by the N2pc (a parieto-occipital electrophysiological component peaking at ∼250 msec). It is unknown, however, if reward associations can similarly modulate attentional shifts to complex objects or object categories, or if reward-related modulation of attentional allocation to such stimuli would occur later in time or through a different mechanism. Here, we used magnetoencephalographic recordings in 24 participants to investigate how object categories with a reward association would modulate the shift of attention. On each trial, two colored squares were presented, one in a target color and the other in a distractor color, each with an embedded object. Participants searched for the target-colored square and performed a corner discrimination task. The embedded objects were from either a rewarded or non-rewarded category, and if a rewarded-category object were present within the target-colored square, participants could earn extra money for correct performance. We observed that when the target color contained an object from a rewarded versus a non-rewarded category, the neural shift of attention to the target was faster and of greater magnitude, although the rewarded objects were not relevant for correct task performance. These results suggest that reward associations of complex objects can rapidly modulate attentional allocation to a target.

Attention to task-relevant features leads to a biasing of sensory selection in extrastriate cortex. Features signaling reward seem to produce a similar bias, but how modulatory effects due to reward and attention relate to each other is largely unexplored. To address this issue, it is critical to separate top–down settings defining reward relevance from those defining attention. To this end, we used a visual search paradigm in which the target's definition (attention to color) was dissociated from reward relevance by delivering monetary reward on search frames where a certain task-irrelevant color was combined with the target-defining color to form the target object. We assessed the state of neural biasing for the attended and reward-relevant color by analyzing the neuromagnetic brain response to asynchronously presented irrelevant distractor probes drawn in the target-defining color, the reward-relevant color, and a completely irrelevant color as a reference. We observed that for the prospect of moderate rewards, the target-defining color but not the reward-relevant color produced a selective enhancement of the neuromagnetic response between 180 and 280 msec in ventral extrastriate visual cortex. Increasing reward prospect caused a delayed attenuation (220–250 msec) of the response to reward probes, which followed a prior (160–180 msec) response enhancement in dorsal ACC. Notably, shorter latency responses in dorsal ACC were associated with stronger attenuation in extrastriate visual cortex. Finally, an analysis of the brain response to the search frames revealed that the presence of the reward-relevant color in search distractors elicited an enhanced response that was abolished after increasing reward size. The present data together indicate that when top–down definitions of reward relevance and attention are separated, the behavioral significance of reward-associated features is still rapidly coded in higher-level cortex areas, thereby commanding effective top–down inhibitory control to counter a selection bias for those features in extrastriate visual cortex.

Attention to one feature of an object can bias the processing of unattended features of that object. Here we demonstrate with ERPs in visual search that this object-based bias for an irrelevant feature also appears in an unattended object when it shares that feature with the target object. Specifically, we show that the ERP response elicited by a distractor object in one visual field is modulated as a function of whether a task-irrelevant color of that distractor is also present in the target object that is presented in the opposite visual field. Importantly, we find this modulation to arise with a delay of approximately 80 msec relative to the N2pc—a component of the ERP response that reflects the focusing of attention onto the target. In a second experiment, we demonstrate that this modulation reflects enhanced neural processing in the unattended object. These observations together facilitate the surprising conclusion that the object-based selection of irrelevant features is spatially global even after attention has selected the target object.

Effective adaptation to the demands of a changing environment requires flexible cognitive control. The medial and the lateral frontal cortices are involved in such control processes, putatively in close interplay with the BG. In particular, dopaminergic projections from the midbrain (i.e., from the substantia nigra [SN] and the ventral tegmental area) have been proposed to play a pivotal role in modulating the activity in these areas for cognitive control purposes. In that dopaminergic involvement has been strongly implicated in reinforcement learning, these ideas suggest functional links between reinforcement learning, where the outcome of actions shapes behavior over time, and cognitive control in a more general context, where no direct reward is involved. Here, we provide evidence from functional MRI in humans that activity in the SN predicts systematic subsequent trial-to-trial RT prolongations that are thought to reflect cognitive control in a stop-signal paradigm. In particular, variations in the activity level of the SN in one trial predicted the degree of RT prolongation on the subsequent trial, consistent with a modulating output signal from the SN being involved in enhancing cognitive control. This link between SN activity and subsequent behavioral adjustments lends support to theoretical accounts that propose dopaminergic control signals that shape behavior both in the presence and in the absence of direct reward. This SN-based modulatory mechanism is presumably mediated via a wider network that determines response speed in this task, including frontal and parietal control regions, along with the BG and the associated subthalamic nucleus.

Faces expressing fear may attract attention in an automatic bottom–up fashion. Here we address this issue with magneto-encephalographic (MEG) recordings in subjects performing a demanding visual search combined with the presentation of irrelevant neutral or fearful faces. The impact of the faces' emotional expression on attentional selection was assessed by analyzing the N2pc component—a modulation of the event-related magnetic field response known to reflect attentional focusing in visual search. We observed that lateralized fearful faces elicited an N2pc approximately between 240 and 400 msec in ventral extrastriate cortex that was independent of the N2pc reflecting target selection in visual search. Despite their clear influence on neural processing, fearful faces did not significantly influence behavioral performance. To clarify this discrepancy, we further performed an MEG experiment in which the demands of the search task were reduced. Under those conditions, lateralized fearful faces elicited an N2pc response that was again independent of the N2pc response to the search target. Behavioral performance was, however, influenced in a significant manner, suggesting that for behavioral effects to appear, sufficient attentional resources need to be left unoccupied by the search task—a notion put forward by the perceptual load theory. Our observations are taken to indicate that irrelevant fearful faces influence attentional processing in extrastriate visual cortex in an automatic fashion and independent of other task-relevant attentional operations. However, this may not necessarily be echoed at the behavioral level as long as task-relevant selection operations exhaust attentional resources.

Knowledge about cause and effect relationships (e.g., virus–epidemic) is essential for predicting changes in the environment and for anticipating the consequences of events and one's own actions. Although there is evidence that predictions and learning from prediction errors are instrumental in acquiring causal knowledge, it is unclear whether prediction error circuitry remains involved in the mental representation and evaluation of causal knowledge already stored in semantic memory. In an fMRI study, participants assessed whether pairs of words were causally related (e.g., virus–epidemic) or noncausally associated (e.g., emerald–ring). In a second fMRI study, a task cue prompted the participants to evaluate either the causal or the noncausal associative relationship between pairs of words. Causally related pairs elicited higher activity in OFC, amygdala, striatum, and substantia nigra/ventral tegmental area than noncausally associated pairs. These regions were also more activated by the causal than by the associative task cue. This network overlaps with the mesolimbic and mesocortical dopaminergic network known to code prediction errors, suggesting that prediction error processing might participate in assessments of causality even under conditions when it is not explicitly required to make predictions.