Dissociating Reward- and Attention-driven Biasing of Global Feature-based Selection in Human Visual Cortex

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.

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Task-Irrelevant Features in Visual Working Memory Influence Covert Attention: Evidence from a Partial Report Task

Vision ◽

10.3390/vision3030042 ◽

2019 ◽

Vol 3 (3) ◽

pp. 42 ◽

Cited By ~ 2

Author(s):

Rebecca M. Foerster ◽

Werner X. Schneider

Keyword(s):

Working Memory ◽

Visual Working Memory ◽

Shape Matching ◽

Target Location ◽

Covert Attention ◽

Partial Report ◽

Target Color ◽

Color Target ◽

Irrelevant Color ◽

Task Irrelevant

Selecting a target based on a representation in visual working memory (VWM) affords biasing covert attention towards objects with memory-matching features. Recently, we showed that even task-irrelevant features of a VWM template bias attention. Specifically, when participants had to saccade to a cued shape, distractors sharing the cue’s search-irrelevant color captured the eyes. While a saccade always aims at one target location, multiple locations can be attended covertly. Here, we investigated whether covert attention is captured similarly as the eyes. In our partial report task, each trial started with a shape-defined search cue, followed by a fixation cross. Next, two colored shapes, each including a letter, appeared left and right from fixation, followed by masks. The letter inside that shape matching the preceding cue had to be reported. In Experiment 1, either target, distractor, both, or no object matched the cue’s irrelevant color. Target-letter reports were most frequent in target-match trials and least frequent in distractor-match trials. Irrelevant cue and target color never matched in Experiment 2. Still, participants reported the distractor more often to the target’s disadvantage, when cue and distractor color matched. Thus, irrelevant features of a VWM template can influence covert attention in an involuntarily object-based manner when searching for trial-wise varying targets.

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Reward- and Attention-related Biasing of Sensory Selection in Visual Cortex

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00539 ◽

2014 ◽

Vol 26 (5) ◽

pp. 1049-1065 ◽

Cited By ~ 19

Author(s):

Antje Buschschulte ◽

Carsten N. Boehler ◽

Hendrik Strumpf ◽

Christian Stoppel ◽

Hans-Jochen Heinze ◽

...

Keyword(s):

Visual Cortex ◽

Target Object ◽

Extrastriate Cortex ◽

Brain Response ◽

Top Down ◽

Extrastriate Visual Cortex ◽

Response Enhancement ◽

Irrelevant Color ◽

Task Irrelevant ◽

Attention To Task

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.

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Global Enhancement but Local Suppression in Feature-based Attention

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01075 ◽

2017 ◽

Vol 29 (4) ◽

pp. 619-627 ◽

Cited By ~ 8

Author(s):

Norman Forschack ◽

Søren K. Andersen ◽

Matthias M. Müller

Keyword(s):

No Reduction ◽

Coherent Motion ◽

Neural Dynamics ◽

Focused Attention ◽

Amplitude Increase ◽

Early Visual Cortex ◽

Feature Based ◽

Left And Right ◽

The One ◽

Task Irrelevant

A key property of feature-based attention is global facilitation of the attended feature throughout the visual field. Previously, we presented superimposed red and blue randomly moving dot kinematograms (RDKs) flickering at a different frequency each to elicit frequency-specific steady-state visual evoked potentials (SSVEPs) that allowed us to analyze neural dynamics in early visual cortex when participants shifted attention to one of the two colors. Results showed amplification of the attended and suppression of the unattended color as measured by SSVEP amplitudes. Here, we tested whether the suppression of the unattended color also operates globally. To this end, we presented superimposed flickering red and blue RDKs in the center of a screen and a red and blue RDK in the left and right periphery, respectively, also flickering at different frequencies. Participants shifted attention to one color of the superimposed RDKs in the center to discriminate coherent motion events in the attended from the unattended color RDK, whereas the peripheral RDKs were task irrelevant. SSVEP amplitudes elicited by the centrally presented RDKs confirmed the previous findings of amplification and suppression. For peripherally located RDKs, we found the expected SSVEP amplitude increase, relative to precue baseline when color matched the one of the centrally attended RDK. We found no reduction in SSVEP amplitude relative to precue baseline, when the peripheral color matched the unattended one of the central RDK, indicating that, while facilitation in feature-based attention operates globally, suppression seems to be linked to the location of focused attention.

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Population Response Profiles in Early Visual Cortex Are Biased in Favor of More Valuable Stimuli

Journal of Neurophysiology ◽

10.1152/jn.01090.2009 ◽

2010 ◽

Vol 104 (1) ◽

pp. 76-87 ◽

Cited By ~ 60

Author(s):

John T. Serences ◽

Sameer Saproo

Keyword(s):

Visual Cortex ◽

Variable Interval ◽

Population Response ◽

Relative Value ◽

Cortical Responses ◽

Response Profile ◽

Early Visual Cortex ◽

Feature Based ◽

Early Effects

Voluntary and stimulus-driven shifts of attention can modulate the representation of behaviorally relevant stimuli in early areas of visual cortex. In turn, attended items are processed faster and more accurately, facilitating the selection of appropriate behavioral responses. Information processing is also strongly influenced by past experience and recent studies indicate that the learned value of a stimulus can influence relatively late stages of decision making such as the process of selecting a motor response. However, the learned value of a stimulus can also influence the magnitude of cortical responses in early sensory areas such as V1 and S1. These early effects of stimulus value are presumed to improve the quality of sensory representations; however, the nature of these modulations is not clear. They could reflect nonspecific changes in response amplitude associated with changes in general arousal or they could reflect a bias in population responses so that high-value features are represented more robustly. To examine this issue, subjects performed a two-alternative forced choice paradigm with a variable-interval payoff schedule to dynamically manipulate the relative value of two stimuli defined by their orientation (one was rotated clockwise from vertical, the other counterclockwise). Activation levels in visual cortex were monitored using functional MRI and feature-selective voxel tuning functions while subjects performed the behavioral task. The results suggest that value not only modulates the relative amplitude of responses in early areas of human visual cortex, but also sharpens the response profile across the populations of feature-selective neurons that encode the critical stimulus feature (orientation). Moreover, changes in space- or feature-based attention cannot easily explain the results because representations of both the selected and the unselected stimuli underwent a similar feature-selective modulation. This sharpening in the population response profile could theoretically improve the probability of correctly discriminating high-value stimuli from low-value alternatives.

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Value-driven attentional capture enhances distractor representations in early visual cortex

10.1101/567354 ◽

2019 ◽

Author(s):

Sirawaj Itthipuripat ◽

Vy A. Vo ◽

Thomas C. Sprague ◽

John T. Serences

Keyword(s):

Visual Cortex ◽

Attentional Capture ◽

Response Selection ◽

Learning Task ◽

Neural Representations ◽

A Value ◽

High Reward ◽

Irrelevant Distractors ◽

Early Visual Cortex ◽

Task Irrelevant

ABSTRACTWhen a behaviorally relevant stimulus has been previously associated with reward, behavioral responses are faster and more accurate compared to equally relevant but less valuable stimuli. Conversely, task irrelevant stimuli that were previously associated with a high reward can capture attention and distract processing away from relevant stimuli (e.g. the chocolate bar in the pantry when you are looking for a nice healthy apple). While increasing the value of task-relevant stimuli systematically up-regulates neural responses in early visual cortex to facilitate information processing, it is not clear if the value of task-irrelevant distractors influences behavior via competition in early visual cortex or via competition at later stages of decision-making and response selection. Here, we measured fMRI in human visual cortex while subjects performed a value-based learning task, and applied a multivariate inverted encoding model to assess the fidelity of distractor representations in early visual cortex. We found that the fidelity of neural representations related to task-irrelevant distractors increased when the distractors were previously associated with a high reward. Moreover, this value-based modulation of distractor representations only occurred when the distractors were previously selected as targets on preceding trials. Together, these findings suggest that value-driven attentional capture begins with sensory modulations of distractor representations in early areas of visual cortex.

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Body shape as a visual feature: evidence from spatially-global attentional modulation in human visual cortex

10.1101/2021.11.17.469004 ◽

2021 ◽

Author(s):

Sushrut Thorat ◽

Marius V. Peelen

Keyword(s):

Visual Cortex ◽

Visual Processing ◽

The Body ◽

Attentional Modulation ◽

Low Level ◽

Object Categories ◽

Feature Based ◽

Vertically Aligned ◽

High Level ◽

Task Irrelevant

Feature-based attention supports the selection of goal-relevant stimuli by enhancing the visual processing of attended features. A defining property of feature-based attention is that it modulates visual processing beyond the focus of spatial attention. Previous work has reported such spatially-global effects for low-level features such as color and orientation, as well as for faces. Here, using fMRI, we provide evidence for spatially-global attentional modulation for human bodies. Participants were cued to search for one of six object categories in two vertically-aligned images. Two additional, horizontally-aligned, images were simultaneously presented but were never task-relevant across three experimental sessions. Analyses time-locked to the objects presented in these task-irrelevant images revealed that responses evoked by body silhouettes were modulated by the participants' top-down attentional set, becoming more body-selective when participants searched for bodies in the task-relevant images. These effects were observed both in univariate analyses of the body-selective cortex and in multivariate analyses of the object-selective visual cortex. Additional analyses showed that this modulation reflected response gain rather than a bias induced by the cues, and that it reflected enhancement of body responses rather than suppression of non-body responses. Finally, the features of early layers of a convolutional neural network trained for object recognition could not be used to accurately categorize body silhouettes, indicating that the fMRI results were unlikely to reflect selection based on low-level features. These findings provide the first evidence for spatially-global feature-based attention for human bodies, linking this modulation to body representations in high-level visual cortex.

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Preparatory Template Activation during Search for Alternating Targets

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01565 ◽

2020 ◽

Vol 32 (8) ◽

pp. 1525-1535

Author(s):

Anna Grubert ◽

Martin Eimer

Keyword(s):

Executive Control ◽

Attentional Control ◽

Time Course ◽

Search Display ◽

Target Color ◽

Target Template ◽

Target Templates ◽

Irrelevant Color ◽

Task Irrelevant ◽

Time Point

Visual search is guided by representations of target-defining features (attentional templates). We tracked the time course of template activation processes during the preparation for search in a task where the identity of color-defined search targets switched across successive trials (ABAB). Task-irrelevant color probes that matched either the upcoming relevant target color or the previous now-irrelevant target color were presented every 200 msec during the interval between search displays. N2pc components (markers of attentional capture) were measured for both types of probes at each time point. A reliable probe N2pc indicates that the corresponding color template is active at the time when the probe appears. N2pcs of equal size emerged from 1000 msec before search display onset for both relevant-color and irrelevant-color probes, demonstrating that both color templates were activated concurrently. Evidence for color-selective attentional control was found only immediately before the arrival of the search display, where N2pcs were larger for relevant-color probes. These results reveal important limitations in the executive control of search preparation in tasks where two targets alternate across trials. Although the identity of the upcoming target is fully predictable, both task-relevant and task-irrelevant target templates are coactivated. Knowledge about target identity selectively biases these template activation processes in a temporally discrete fashion, guided by temporal expectations about when the target template will become relevant.

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