Carsten N. Boehler

Pinning down response inhibition in the brain — Conjunction analyses of the Stop-signal task

Successful behavior requires a finely-tuned interplay of initiating and inhibiting motor programs to react effectively to constantly changing environmental demands. One particularly useful paradigm for investigating inhibitory motor control is the Stop-signal task, where already-initiated responses to Go-stimuli are to be inhibited upon the rapid subsequent presentation of a Stop-stimulus (yielding successful and unsuccessful Stop-trials). Despite the extensive use of this paradigm in functional neuroimaging, there is no consensus on which functional comparison to use to characterize response-inhibition-related brain activity. Here, we utilize conjunction analyses of successful and unsuccessful Stop-trials that are each contrasted against a reference condition. This conjunction approach identifies processes common to both Stop-trial types while excluding processes specific to either, thereby capitalizing on the presence of some response-inhibition-related activity in both conditions. Using this approach on fMRI data from human subjects, we identify a network of brain structures that was linked to both types of Stop-trials, including lateral-inferior frontal and medial frontal cortical areas and the caudate nucleus. In addition, comparisons with a reference condition matched for visual stimulation identified additional activity in the right inferior parietal cortex that may play a role in enhancing the processing of the Stop-stimuli. Finally, differences in stopping efficacy across subjects were associated with variations in activity in the left anterior insula. However, this region was also associated with general task accuracy (which furthermore correlated directly with stopping efficacy), suggesting that it might actually reflect a more general mechanism of performance control that supports response inhibition in a relatively nonspecific way.

The influence of reward associations on conflict processing in the Stroop task

Performance in a behavioral task can be facilitated by associating stimulus properties with reward. In contrast, conflicting information is known to impede task performance. Here we investigated how reward associations influence the within-trial processing of conflicting information using a color-naming Stroop task in which a subset of ink colors (task-relevant dimension) was associated with monetary incentives. We found that color-naming performance was enhanced on trials with potential-reward versus those without. Moreover, in potential-reward trials, typical conflict-induced performance decrements were attenuated if the incongruent word (task-irrelevant dimension) was unrelated to reward. In contrast, incongruent words that were semantically related to reward-predicting ink colors interfered with performance in potential-reward trials and even more so in no-reward trials, despite the semantic meaning being entirely task-irrelevant. These observations imply that the prospect of reward enhances the processing of task-relevant stimulus information, whereas incongruent reward-related information in a task-irrelevant dimension can impede task performance.

The Involvement of the Dopaminergic Midbrain and Cortico-Striatal-Thalamic Circuits in the Integration of Reward Prospect and Attentional Task Demands

Reward has been shown to promote human performance in multiple task domains. However, an important debate has developed about the uniqueness of reward-related neural signatures associated with such facilitation, as similar neural patterns can be triggered by increased attentional focus independent of reward. Here, we used functional magnetic resonance imaging to directly investigate the neural commonalities and interactions between the anticipation of both reward and task difficulty, by independently manipulating these factors in a cued-attention paradigm. In preparation for the target stimulus, both factors increased activity within the midbrain, dorsal striatum, and fronto-parietal areas, while inducing deactivations in default-mode regions. Additionally, reward engaged the ventral striatum, posterior cingulate, and occipital cortex, while difficulty engaged medial and dorsolateral frontal regions. Importantly, a network comprising the midbrain, caudate nucleus, thalamus, and anterior midcingulate cortex exhibited an interaction between reward and difficulty, presumably reflecting additional resource recruitment for demanding tasks with profitable outcome. This notion was consistent with a negative correlation between cue-related midbrain activity and difficulty-induced performance detriments in reward-predictive trials. Together, the data demonstrate that expected value and attentional demands are integrated in cortico-striatal-thalamic circuits in coordination with the dopaminergic midbrain to flexibly modulate resource allocation for an effective pursuit of behavioral goals.

Rapid recurrent processing gates awareness in primary visual cortex

Visual awareness has been proposed to depend on recurrent processing in early visual cortex areas including the primary visual cortex (V1). Here, we address this hypothesis with high spatiotemporal resolution magnetoencephalographic recordings in subjects performing a substitution masking paradigm. Neural activity reflecting awareness is assessed by directly comparing the neuromagnetic response elicited by effectively and ineffectively masked targets after the proportion of trials leading to masking was individually adjusted to match the proportion of trials without masking. This revealed a modulation of recurrent activity in the primary visual cortex rapidly after the onset of the feedforward sweep of processing in striate and extrastriate areas but significantly before the onset of attention-dependent recurrent modulations in V1. Our data provide direct support for the notion that (i) recurrent processing in V1 correlates with visual awareness and (ii) that attention and awareness involve distinct recurrent processing operations.

The Neural Site of Attention Matches the Spatial Scale of Perception

What is the neural locus of visual attention? Here we show that the locus is not fixed but instead changes rapidly to match the spatial scale of task-relevant information in the current scene. To accomplish this, we obtained electrical, magnetic, and hemodynamic measures of attention from human subjects while they detected large-scale or small-scale targets within multiscale stimulus patterns. Subjects did not know the scale of the target before stimulus onset, and yet the neural locus of attention-related activity between 250 and 300 ms varied according to the scale of the target. Specifically, maximal attention-related activity spread from a high-level, relatively anterior visual area (the lateral occipital complex) for large-scale targets to include a lower-level, more posterior area (visual area V4) for small-scale targets. This rapid change indicates that the neural locus of attention in visual cortex is not static but is instead determined rapidly and dynamically by means of an interaction between top-down task information and local information about the current visual input.

Sound-induced enhancement of low-intensity vision: Multisensory influences on human sensory-specific cortices and thalamic bodies relate to perceptual enhancement of visual detection sensitivity

Combining information across modalities can affect sensory performance. We studied how co-occurring sounds modulate behavioral visual detection sensitivity (d′), and neural responses, for visual stimuli of higher or lower intensity. Co-occurrence of a sound enhanced human detection sensitivity for lower- but not higher-intensity visual targets. Functional magnetic resonance imaging (fMRI) linked this to boosts in activity-levels for sensory-specific visual and auditory cortex, plus multisensory superior temporal sulcus (STS), specifically for a lower-intensity visual event when paired with a sound. Thalamic structures in visual and auditory pathways, the lateral and medial geniculate bodies, respectively (LGB, MGB), showed a similar pattern. Subject-by-subject psychophysical benefits correlated with corresponding fMRI signals in visual, auditory, and multisensory regions. We also analyzed differential “coupling” patterns of LGB and MGB with other regions in the different experimental conditions. Effective-connectivity analyses showed enhanced coupling of sensory-specific thalamic bodies with the affected cortical sites during enhanced detection of lower-intensity visual events paired with sounds. Coupling strength between visual and auditory thalamus with cortical regions, including STS, covaried parametrically with the psychophysical benefit for this specific multisensory context. Our results indicate that multisensory enhancement of detection sensitivity for low-contrast visual stimuli by co-occurring sounds reflects a brain network involving not only established multisensory STS and sensory-specific cortex but also visual and auditory thalamus.

The neural underpinnings of how reward associations can both guide and misguide attention

It is commonly accepted that reward is an effective motivator of behavior, but little is known about potential costs resulting from reward associations. Here, we used functional magnetic resonance imaging (fMRI) to investigate the neural underpinnings of such reward-related performance-disrupting effects in a reward-modulated Stroop task in humans. While reward associations in the task-relevant dimension (i.e., ink color) facilitated performance, behavioral detriments were found when the task-irrelevant dimension (i.e., word meaning) implicitly referred to reward-predictive ink colors. Neurally, only relevant reward associations invoked a typical reward-anticipation response in the nucleus accumbens (NAcc), which was in turn predictive of behavioral facilitation. In contrast, irrelevant reward associations increased activity in a medial prefrontal motor-control-related region, namely the presupplementary motor area (pre-SMA), which likely reflects the preemption and inhibition of automatic response tendencies that are amplified by irrelevant reward-related words. This view was further supported by a positive relationship between pre-SMA activity and pronounced response slowing in trials containing reward-related as compared with reward-unrelated incongruent words. Importantly, the distinct neural processes related to the beneficial and detrimental behavioral effects of reward associations appeared to arise from preferential-coding mechanisms in visual-processing areas that were shared by the two stimulus dimensions, suggesting a transfer of reward-related saliency to the irrelevant dimension, but with highly differential behavioral and neural ramifications. More generally, the data demonstrate that even entirely irrelevant reward associations can influence stimulus-processing and response-selection pathways relatively automatically, thereby representing an important flipside of reward-driven performance enhancements.

The heterogeneous world of congruency sequence effects: an update

Congruency sequence effects (CSEs) refer to the observation that congruency effects in conflict tasks are typically smaller following incongruent compared to following congruent trials. This measure has long been thought to provide a unique window into top-down attentional adjustments and their underlying brain mechanisms. According to the renowned conflict monitoring theory, CSEs reflect enhanced selective attention following conflict detection. Still, alternative accounts suggested that bottom-up associative learning suffices to explain the pattern of reaction times and error rates. A couple of years ago, a review by Egner (2007) pitted these two rivalry accounts against each other, concluding that both conflict adaptation and feature integration contribute to the CSE. Since then, a wealth of studies has further debated this issue, and two additional accounts have been proposed, offering intriguing alternative explanations. Contingency learning accounts put forward that predictive relationships between stimuli and responses drive the CSE, whereas the repetition expectancy hypothesis suggests that top-down, expectancy-driven control adjustments affect the CSE. In the present paper, we build further on the previous review (Egner, 2007) by summarizing and integrating recent behavioral and neurophysiological studies on the CSE. In doing so, we evaluate the relative contribution and theoretical value of the different attentional and memory-based accounts. Moreover, we review how all of these influences can be experimentally isolated, and discuss designs and procedures that can critically judge between them.

Task-load-dependent activation of dopaminergic midbrain areas in the absence of reward

Dopamine release in cortical and subcortical structures plays a central role in reward-related neural processes. Within this context, dopaminergic inputs are commonly assumed to play an activating role, facilitating behavioral and cognitive operations necessary to obtain a prospective reward. Here, we provide evidence from human fMRI that this activating role can also be mediated by task-demand-related processes and thus extends beyond situations that only entail extrinsic motivating factors. Using a visual discrimination task in which varying levels of task demands were precued, we found enhanced hemodynamic activity in the substantia nigra (SN) for high task demands in the absence of reward or similar extrinsic motivating factors. This observation thus indicates that the SN can also be activated in an endogenous fashion. In parallel to its role in reward-related processes, reward-independent activation likely serves to recruit the processing resources needed to meet enhanced task demands. Simultaneously, activity in a wide network of cortical and subcortical control regions was enhanced in response to high task demands, whereas areas of the default-mode network were deactivated more strongly. The present observations suggest that the SN represents a core node within a broader neural network that adjusts the amount of available neural and behavioral resources to changing situational opportunities and task requirements, which is often driven by extrinsic factors but can also be controlled endogenously.

The Center-Surround Profile of the Focus of Attention Arises from Recurrent Processing in Visual Cortex

We recently demonstrated with magnetoencephalographic recordings in human observers that the focus of attention in visual search has a spatial profile consisting of a center enhancement surrounded by a narrow zone of sensory attenuation. Here, we report new data from 2 experiments providing insights into the cortical processes that cause the surround attenuation. We show that surround suppression appears in search tasks that require spatial scrutiny, that is the precise binding of search-relevant features at the targets location but not in tasks that permit target discrimination without precise localization. Furthermore, we demonstrate that surround attenuation is linked with a stronger recurrent activity modulation in early visual cortex. Finally, we show that surround suppression appears with a delay (more than 175 ms) that is beyond the time course of the initial feedforward sweep of processing in the visual system. These observations together indicate that the suppressive surround is associated with recurrent processing and binding in the visual cortex.