Statistical Learning of Distractor Suppression Downregulates Prestimulus Neural Excitability in Early Visual Cortex.

Visual attention is highly influenced by past experiences. Recent behavioral research has shown that expectations about the spatial location of distractors within a search array are implicitly learned, with expected distractors becoming less interfering. Little is known about the neural mechanism supporting this form of statistical learning. Here, we used magnetoencephalography (MEG) to measure human brain activity to test whether proactive mechanisms are involved in the statistical learning of distractor locations. Specifically, we used a new technique called rapid invisible frequency tagging (RIFT) to assess neural excitability in early visual cortex during statistical learning of distractor suppression while concurrently investigating the modulation of posterior alpha band activity (8-12 Hz). Male and female human participants performed a visual search task in which a target was occasionally presented alongside a color-singleton distractor. Unbeknown to the participants, the distracting stimuli were presented with different probabilities across the two hemifields. RIFT analysis showed that early visual cortex exhibited reduced neural excitability in the prestimulus interval at retinotopic locations associated with higher distractor probabilities. In contrast, we did not find any evidence of expectation-driven distractor suppression in alpha band activity. These findings indicate that proactive mechanisms of attention are involved in predictive distractor suppression and that these mechanisms are associated with altered neural excitability in early visual cortex. Moreover, our findings indicate that RIFT and alpha band activity might subtend different and possibly independent attentional mechanisms.SIGNIFICANCE STATEMENT What we experienced in the past affects how we perceive the external world in the future. For example, an annoying flashing light might be better ignored if we know in advance where it usually appears. This ability of extracting regularities from the environment is called statistical learning. In this study, we explore the neuronal mechanisms allowing the attentional system to overlook items that are unequivocally distracting based on their spatial distribution. By recording brain activity using MEG while probing neural excitability with a novel technique called RIFT, we show that the neuronal excitability in early visual cortex is reduced in advance of stimulus presentation for locations where distracting items are more likely to occur.

FLUX: A pipeline for MEG analysis.

Magnetoencephalography (MEG) allows for quantifying modulations of human neuronal activity on a millisecond time scale while also making it possible to estimate the location of the underlying neuronal sources. The technique relies heavily on signal processing and source modelling. To this end, there are several open-source toolboxes developed by the community. While these toolboxes are powerful as they provide a wealth of options for analyses, the many options also pose a challenge for reproducible research as well as for researchers new to the field. The FLUX pipeline aims to make the analyses steps and setting explicit for standard analysis done in cognitive neuroscience. It focuses on quantifying and source localization of oscillatory brain activity, but it can also be used for event-related fields and multivariate pattern analysis. The pipeline is derived from the Cogitate consortium addressing a set of concrete cognitive neuroscience questions. Specifically, the pipeline including documented code is defined for MNE Python (a Python toolbox) and FieldTrip (a Matlab toolbox), and a data set on visuospatial attention is used to illustrate the steps. The scripts are provided as notebooks implemented in Jupyter Notebook and MATLAB Live Editor providing explanations, justifications and graphical outputs for the essential steps. Furthermore, we also provide suggestions for text and parameter settings to be used in registrations and publications to improve replicability and facilitate pre-registrations. The FLUX can be used for education either in self-studies or guided workshops. We expect that the FLUX pipeline will strengthen the field of MEG by providing some standardization on the basic analysis steps and by aligning approaches across toolboxes. Furthermore, we also aim to support new researchers entering the field by providing education and training. The FLUX pipeline is not meant to be static; it will evolve with the development of the toolboxes and with new insights. Furthermore, with the anticipated increase in MEG systems based on the Optically Pumped Magnetometers, the pipeline will also evolve to embrace these developments.

Body-Space Interactions: Same Spatial Encoding but Different Influence of Valence for Reaching and Defensive Purposes.

The space around our body, the so-called peripersonal space, is where interactions with nearby objects may occur. "Defensive space" and "Reaching space", respectively, refer to two opposite poles of interaction between our body and the external environment: protecting the body and performing a goal-directed action. Here, we hypothesized that mechanisms underlying these two action spaces are differentially modulated by the valence of visual stimuli, as stimuli with negative valence are more likely to activate protective actions whereas stimuli with positive valence may activate approaching actions. To test whether such distinction in cognitive/evaluative processing exists between Reaching and Defensive spaces, we measured behavioral responses as well as neural activations over sensorimotor cortex using EEG while participants performed several tasks designed to tap into mechanisms underlying either Defensive (e.g., respond to touch) or Reaching space (e.g., estimate whether object is within reaching distance). During each task, pictures of objects with either positive or negative valence were presented at different distances from the participants' body. We found that Defensive space was smaller for positively compared with negatively valenced visual stimuli. Furthermore, sensorimotor cortex activation (reflected in modulation of beta power) during tactile processing was enhanced when coupled with negatively rather than positively valenced visual stimuli regarding Defensive space. On the contrary, both the EEG and behavioral measures capturing the mechanisms underlying Reaching space did not reveal any modulation by valence. Thus, although valence encoding had differential effects on Reaching and Defensive spaces, the distance of the visual stimulus modulated behavioral measures as well as activity over sensorimotor cortex (reflected in modulations of mu power) in a similar way for both types of spaces. Our results are compatible with the idea that Reaching and Defensive spaces involve the same distance-dependent neural representations of sensory input, whereas task goals and stimulus valence (i.e., contextual information) are implemented at a later processing stage and exert an influence on motor output rather than sensory/space encoding.

Probing the Neural Mechanisms for Distractor Filtering and Their History-Contingent Modulation by Means of TMS.

In visual search, the presence of a salient, yet task-irrelevant, distractor in the stimulus array interferes with target selection and slows down performance. Neuroimaging data point to a key role of the frontoparietal dorsal attention network in dealing with visual distractors; however, the respective roles of different nodes within the network and their hemispheric specialization are still unresolved. Here, we used transcranial magnetic stimulation (TMS) to evaluate the causal role of two key regions of the dorsal attention network in resisting attentional capture by a salient singleton distractor: the frontal eye field (FEF) and the cortex within the intraparietal sulcus (IPS). The task of the participants (male/female human volunteers) was to discriminate the pointing direction of a target arrow while ignoring a task-irrelevant salient distractor. Immediately after stimulus onset, triple-pulse 10 Hz TMS was delivered either to IPS or FEF on either side of the brain. Results indicated that TMS over the right FEF significantly reduced the behavioral cost engendered by the salient distractor relative to left FEF stimulation. No such effect was obtained with stimulation of IPS on either side of brain. Interestingly, this FEF-dependent reduction in distractor interference interacted with the contingent trial history, being maximal when no distractor was present on the previous trial relative to when there was one. Our results provide direct causal evidence that the right FEF houses key mechanisms for distractor filtering, pointing to a pivotal role of the frontal cortex of the right hemisphere in limiting interference from an irrelevant but attention-grabbing stimulus.SIGNIFICANCE STATEMENT Visually conspicuous stimuli attract our attention automatically and interfere with performance by diverting resources away from the main task. Here, we applied transcranial magnetic stimulation over four frontoparietal cortex locations (frontal eye field and intraparietal sulcus in each hemisphere) to identify regions of the dorsal attention network that help limit interference from task-irrelevant, salient distractors. Results indicate that the right FEF participates in distractor-filtering mechanisms that are recruited when a distracting stimulus is encountered. Moreover, right FEF implements adjustments in distraction-filtering mechanisms following recent encounters with distractors. Together, these findings indicate a different hemispheric contribution of the left versus right dorsal frontal cortex to distraction filtering. This study expands our understanding of how our brains select relevant targets in the face of task-irrelevant, salient distractors.

Prefrontal cortex oscillations update and stabilize consciousness during binocular rivalry.

In this issue of Neuron, Dwarakanath et al.1 demonstrate that perceptual changes in binocular rivalry are predicted by low-frequency activity and beta-band oscillations in the prefrontal cortex, speaking to access consciousness being gated by oscillatory neuronal dynamics in the prefrontal cortex.

Statistical learning of target and distractor spatial probability shape a common attentional priority computation.

Converging evidence recently put forward the notion that dedicated neurocognitive mechanisms do exist for the suppression of salient, but irrelevant distractors. Along this line, it is plausible to hypothesize that, in appropriate contexts, experience-dependent forms of attentional learning might selectively induce plastic changes within this dedicated circuitry, thus allowing an independent shaping of priorities at the service of attentional filtering. Conversely, previous work suggested that statistical learning (SL) of both target and distractor spatial probability distributions converge in adjusting only the overall attentional priority of locations: in fact, in the presence of an independent manipulation, either related to the target or to the distractor only, SL induces indirect effects (e.g., changes in filtering efficiency due to an uneven distribution of targets), suggesting that SL-induced plastic changes affect a shared neural substrate. Here we tested whether, when (conflicting) target- and distractor-related manipulations are concurrently applied to the very same locations, dedicated mechanisms might support the selective encoding of spatial priority in relation to the specific attentional operation involved. In three related experiments, human healthy participants discriminated the direction of a target arrow, while ignoring a salient distractor, if present; both target and distractor spatial probability distributions were concurrently manipulated in relation to each single location. Critically, the selection bias produced by the target-related SL was marginally reduced by an adverse distractor contingency, and the suppression bias generated by the distractor-related SL was erased, or even reversed, by an adverse target contingency. Our results suggest that even conflicting target- and distractor-related SL manipulations result in the adjustment of a unique spatial priority computation, likely because the process directly relies on direct plastic alterations of shared spatial priority map(s).

An adversarial collaboration protocol for testing contrasting predictions of global neuronal workspace and integrated information theory.

The relationship between conscious experience and brain activity has intrigued scientists and philosophers for centuries. In the last decades, several theories have suggested different accounts for these relationships. These theories have developed in parallel, with little to no cross-talk among them. To advance research on consciousness, we established an adversarial collaboration between proponents of two of the major theories in the field, Global Neuronal Workspace and Integrated Information Theory. Together, we devised and preregistered two experiments that test contrasting predictions of these theories concerning the location and timing of correlates of visual consciousness, which have been endorsed by the theories' proponents. Predicted outcomes should either support, refute, or challenge these theories. Six theory-impartial laboratories will follow the study protocol specified here, using three complementary methods: Functional Magnetic Resonance Imaging (fMRI), Magneto-Electroencephalography (M-EEG), and intracranial electroencephalography (iEEG). The study protocol will include built-in replications, both between labs and within datasets. Through this ambitious undertaking, we hope to provide decisive evidence in favor or against the two theories and clarify the footprints of conscious visual perception in the human brain, while also providing an innovative model of large-scale, collaborative, and open science practice.

Modulating the influence of recent trial history on attentional capture via transcranial magnetic stimulation (TMS) of right TPJ.

In visual search, salient yet task-irrelevant distractors in the stimulus array interfere with target selection. This is due to the unwanted shift of attention towards the salient stimulus-the so-called attentional capture effect, which delays deployment of attention onto the target. Although powerful and automatic, attentional capture by a salient distractor is nonetheless antagonized by distractor-filtering mechanisms and is further modulated by cross-trial contingencies: The distractor cost is typically more robust when no distraction has been experienced in the immediate past, compared to when a distractor was present on the immediately preceding trial. Here, we used transcranial magnetic stimulation (TMS) to shed light on the causal role of two crucial nodes of the ventral attention network, namely the Temporo-Parietal Junction (TPJ) and the Middle Frontal Gyrus (MFG), in the exogenous control of attention (i.e., attentional capture) and its history-dependent modulation. Participants were asked to discriminate the direction of a target arrow while ignoring a task-irrelevant salient distractor, when present. Immediately after display onset, 10 Hz triple-pulse TMS was delivered either to TPJ or MFG on the right hemisphere. Results demonstrated that stimulation of right TPJ-but not of right MFG, strongly modulated attentional capture as a function of the type of previous trial, by somewhat enhancing the distractor-related cost when the preceding trial was a distractor-absent trial and significantly decreasing the cost when the preceding trial was a distractor-present trial. These findings indicate that TMS of right TPJ exacerbates the effect of the recent history, likely reflecting enhanced updating of the predictive model that dynamically governs proactive distractor-filtering mechanisms. More generally, the results attest to a role of TPJ in mediating the history-dependent modulation of attentional capture.

Altering spatial priority maps via statistical learning of target selection and distractor filtering.

The cognitive system has the capacity to learn and make use of environmental regularities - known as statistical learning (SL), including for the implicit guidance of attention. For instance, it is known that attentional selection is biased according to the spatial probability of targets; similarly, changes in distractor filtering can be triggered by the unequal spatial distribution of distractors. Open questions remain regarding the cognitive/neuronal mechanisms underlying SL of target selection and distractor filtering. Crucially, it is unclear whether the two processes rely on shared neuronal machinery, with unavoidable cross-talk, or they are fully independent, an issue that we directly addressed here. In a series of visual search experiments, participants had to discriminate a target stimulus, while ignoring a task-irrelevant salient distractor (when present). We systematically manipulated spatial probabilities of either one or the other stimulus, or both. We then measured performance to evaluate the direct effects of the applied contingent probability distribution (e.g., effects on target selection of the spatial imbalance in target occurrence across locations) as well as its indirect or "transfer" effects (e.g., effects of the same spatial imbalance on distractor filtering across locations). By this approach, we confirmed that SL of both target and distractor location implicitly bias attention. Most importantly, we described substantial indirect effects, with the unequal spatial probability of the target affecting filtering efficiency and, vice versa, the unequal spatial probability of the distractor affecting target selection efficiency across locations. The observed cross-talk demonstrates that SL of target selection and distractor filtering are instantiated via (at least partly) shared neuronal machinery, as further corroborated by strong correlations between direct and indirect effects at the level of individual participants. Our findings are compatible with the notion that both kinds of SL adjust the priority of specific locations within attentional priority maps of space.