Spatial attention has been postulated to facilitate perceptual processing via several different mechanisms. For instance, attention can amplify neural responses in sensory areas (sensory gain), mediate neural variability (noise modulation), or alter the manner in which sensory signals are selectively read out by postsensory decision mechanisms (efficient readout). Even in the context of simple behavioral tasks, it is unclear how well each of these mechanisms can account for the relationship between attention-modulated changes in behavior and neural activity because few studies have systematically mapped changes between stimulus intensity, attentional focus, neural activity, and behavioral performance. Here, we used a combination of psychophysics, event-related potentials (ERPs), and quantitative modeling to explicitly link attention-related changes in perceptual sensitivity with changes in the ERP amplitudes recorded from human observers. Spatial attention led to a multiplicative increase in the amplitude of an early sensory ERP component (the P1, peaking ϳ80 -130 ms poststimulus) and in the amplitude of the late positive deflection component (peaking ϳ230 -330 ms poststimulus). A simple model based on signal detection theory demonstrates that these multiplicative gain changes were sufficient to account for attention-related improvements in perceptual sensitivity, without a need to invoke noise modulation. Moreover, combining the observed multiplicative gain with a postsensory readout mechanism resulted in a significantly poorer description of the observed behavioral data. We conclude that, at least in the context of relatively simple visual discrimination tasks, spatial attention modulates perceptual sensitivity primarily by modulating the gain of neural responses during early sensory processing
It has been proposed that working memory (WM) is updated/manipulated via a fronto-basal-ganglia circuit. One way that this could happen is via the synchronization of neural oscillations. A first step towards testing this hypothesis is to clearly establish a frontal scalp EEG signature of WM manipulation. Although many EEG studies have indeed revealed frontal EEG signatures for WM, especially in the theta frequency band (3–8 Hz), few of them required subjects to manipulate WM, and of those that did, none specifically tied the EEG signature to the manipulation process per se. Here we employed a WM manipulation task that has been shown with imaging to engage the prefrontal cortex and the striatum. We adapted this task to titrate the success of WM manipulation to approximately 50%. Using time-frequency analysis of EEG, we showed that theta power is increased over frontal cortex for successful versus failed WM manipulation, specifically at the time of the manipulation event. This establishes a clear-cut EEG signature of WM manipulation. Future studies could employ this to test the fronto-basal-ganglia hypothesis of WM updating/manipulation.
Over the last several decades, spatial attention has been shown to influence the activity of neurons in visual cortex in various ways. These conflicting observations have inspired competing models to account for the influence of attention on perception and behavior. Here, we used electroencephalography (EEG) to assess steady-state visual evoked potentials (SSVEP) in human subjects and showed that highly focused spatial attention primarily enhanced neural responses to high-contrast stimuli (response gain), whereas distributed attention primarily enhanced responses to medium-contrast stimuli (contrast gain). Together, these data suggest that different patterns of neural modulation do not reflect fundamentally different neural mechanisms, but instead reflect changes in the spatial extent of attention.
Two factors play important roles in shaping perception: the allocation of selective attention to behaviorally relevant sensory features, and prior expectations about regularities in the environment. Signal detection theory proposes distinct roles of attention and expectation on decision-making such that attention modulates early sensory processing, whereas expectation influences the selection and execution of motor responses. Challenging this classic framework, recent studies suggest that expectations about sensory regularities enhance the encoding and accumulation of sensory evidence during decision-making. However, it is possible, that these findings reflect well documented attentional modulations in visual cortex. Here, we tested this framework in a group of male and female human participants by examining how expectations about stimulus features (orientation and color) and expectations about motor responses impacted electroencephalography (EEG) markers of early sensory processing and the accumulation of sensory evidence during decision-making (the early visual negative potential and the centro-parietal positive potential, respectively). We first demonstrate that these markers are sensitive to changes in the amount of sensory evidence in the display. Then we show, counter to recent findings, that neither marker is modulated by either feature or motor expectations, despite a robust effect of expectations on behavior. Instead, violating expectations about likely sensory features and motor responses impacts posterior alpha and frontal theta oscillations, signals thought to index overall processing time and cognitive conflict. These findings are inconsistent with recent theoretical accounts and suggest instead that expectations primarily influence decisions by modulating post-perceptual stages of information processing. Expectations about likely features or motor responses play an important role in shaping behavior. Classic theoretical frameworks posit that expectations modulate decision-making by biasing late stages of decision-making including the selection and execution of motor responses. In contrast, recent accounts suggest that expectations also modulate decisions by improving the quality of early sensory processing. However, these effects could instead reflect the influence of selective attention. Here we examine the effect of expectations about sensory features and motor responses on a set of electroencephalography (EEG) markers that index early sensory processing and later post-perceptual processing. Counter to recent empirical results, expectations have little effect on early sensory processing but instead modulate EEG markers of time-on-task and cognitive conflict.
Functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) are two noninvasive methods commonly used to study neural mechanisms supporting visual attention in humans. Studies using these tools, which have complementary spatial and temporal resolutions, implicitly assume they index similar underlying neural modulations related to external stimulus and internal attentional manipulations. Accordingly, they are often used interchangeably for constraining understanding about the impact of bottom-up and top-down factors on neural modulations. To test this core assumption, we simultaneously manipulated bottom-up sensory inputs by varying stimulus contrast and top-down cognitive modulations by changing the focus of spatial attention. Each of the male and female subjects participated in both fMRI and EEG sessions performing the same experimental paradigm. We found categorically different patterns of attentional modulation on fMRI activity in early visual cortex and early stimulus-evoked potentials measured via EEG (e.g., the P1 component and steady-state visually-evoked potentials): fMRI activation scaled additively with attention, whereas evoked EEG components scaled multiplicatively with attention. However, across longer time scales, a contralateral negative-going potential and oscillatory EEG signals in the alpha band revealed additive attentional modulation patterns like those observed with fMRI. These results challenge prior assumptions that fMRI and early stimulus-evoked potentials measured with EEG can be interchangeably used to index the same neural mechanisms of attentional modulations at different spatiotemporal scales. Instead, fMRI measures of attentional modulations are more closely linked with later EEG components and alpha-band oscillations. Considered together, hemodynamic and electrophysiological signals can jointly constrain understanding of the neural mechanisms supporting cognition.
Normative theories posit that value-based decision-making is context independent. However, decisions between two high-value options can be suboptimally biased by the introduction of a third low-value option. This context-dependent modulation is consistent with the divisive normalization of the value of each stimulus by the total value of all stimuli. In addition, an independent line of research demonstrates that pairing a stimulus with a high-value outcome can lead to attentional capture that can mediate the efficiency of visual information processing. Here we tested the hypothesis that value-based attentional capture interacts with value-based normalization to influence the optimality of decision-making. We used a binary-choice paradigm in which observers selected between two targets and the color of each target indicated the magnitude of their reward potential. Observers also had to simultaneously ignore a task-irrelevant distractor rendered in a color that was previously associated with a specific reward magnitude. When the color of the task-irrelevant distractor was previously associated with a high reward, observers responded more slowly and less optimally. Moreover, as the learned value of the distractor increased, electrophysiological data revealed an attenuation of the lateralized N1 and N2Pc responses evoked by the relevant choice stimuli and an attenuation of the late positive deflection (LPD). Collectively, these behavioral and electrophysiological data suggest that value-based attentional capture and value-based normalization jointly mediate the influence of context on free-choice decision-making.
Computational models posit that visual attention is guided by activity within spatial maps that index the image-computable salience and the behavioral relevance of objects in the scene. These spatial maps are theorized to be instantiated as activation patterns across a series of retinotopic visual regions in occipital, parietal, and frontal cortex. Whereas previous research has identified sensitivity to either the behavioral relevance or the image-computable salience of different scene elements, the simultaneous influence of these factors on neural "attentional priority maps" in human cortex is not well understood. We tested the hypothesis that visual salience and behavioral relevance independently impact the activation profile across retinotopically organized cortical regions by quantifying attentional priority maps measured in human brains using functional MRI while participants attended one of two differentially salient stimuli. We found that the topography of activation in priority maps, as reflected in the modulation of region-level patterns of population activity, independently indexed the physical salience and behavioral relevance of each scene element. Moreover, salience strongly impacted activation patterns in early visual areas, whereas later visual areas were dominated by relevance. This suggests that prioritizing spatial locations relies on distributed neural codes containing graded representations of salience and relevance across the visual hierarchy. NEW & NOTEWORTHY We tested a theory which supposes that neural systems represent scene elements according to both their salience and their relevance in a series of "priority maps" by measuring functional MRI activation patterns across human brains and reconstructing spatial maps of the visual scene. We found that different regions indexed either the salience or the relevance of scene items, but not their interaction, suggesting an evolving representation of salience and relevance across different visual areas.
Although attention is known to improve the efficacy of sensory processing, the impact of attention on subjective visual appearance is still a matter of debate. Although recent studies suggest that attention can alter the appearance of stimulus contrast, others argue that these changes reflect response bias induced by attention cues. Here, we provide evidence that attention has effects on both appearance and response bias. In a comparative judgment task in which subjects reported whether the attended or unattended visual stimulus had a higher perceived contrast, attention induced substantial baseline-offset response bias as well as small but significant changes in subjective contrast appearance when subjects viewed near-threshold stimuli. However, when subjects viewed suprathreshold stimuli, baseline-offset response bias decreased and attention primarily changed contrast appearance. To address the possibility that these changes in appearance might be influenced by uncertainty due to the attended and unattended stimuli having similar physical contrasts, subjects performed an equality judgment task in which they reported if the contrast of the two stimuli was the same or different. We found that, although there were still attention-induced changes in contrast appearance at lower contrasts, the robust changes in contrast appearance at higher contrasts observed in the comparative judgment task were diminished in the equality judgment task. Together, these results suggest that attention can impact both response bias and appearance, and these two types of attention effects are differentially mediated by stimulus visibility and uncertainty. Collectively, these findings help constrain arguments about the cognitive penetrability of perception.
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