Fear in action: Fear conditioning and alleviation through body movements.

Fear memories enhance survival especially when the memories guide defensive movements to minimize harm. Accordingly, fear memories and body movements have tight relationships in animals: Fear memory acquisition results in adapting reactive defense movements, while training active defense movements reduces fear memory. However, evidence in humans is scarce because their movements are typically suppressed in experiments. Here, we tracked adult participants' body motions while they underwent ecologically valid fear conditioning in a 3D virtual space. First, with body motion tracking, we revealed that distinct spatiotemporal body movement patterns emerge through fear conditioning. Second, subsequent training to actively avoid threats with naturalistic defensive actions led to a long-term (24 h) reduction of physiological and embodied conditioned responses, while extinction or vicarious training only transiently reduced the responses. Together, our results highlight the role of body movements in human fear memory and its intervention.

Evidence for Transcranial Magnetic Stimulation Induced Functional Connectivity Oscillations in the Brain.

Transcranial magnetic stimulation (TMS) is an effective research tool to elucidate mechanisms of function in the brain. Despite its widespread use, very few studies have looked at dynamic functional connectivity responses to TMS. This work performs an exploratory analysis of dynamic functional network connectivity (dynFNC) to evaluate evidence of brain response to TMS. Results show clear functional dynamic patterns categorized by frequency. Some patterns appear to be more directly linked to TMS, but there is one pattern that might be a TMS-independent response to the excitation. This first look presents an analysis methodology and important results to consider in future research.

Transcranial magnetic stimulation alters multivoxel patterns in the absence of overall activity changes.

Transcranial magnetic stimulation (TMS) has become one of the major tools for establishing the causal role of specific brain regions in perceptual, motor, and cognitive processes. Nevertheless, a persistent limitation of the technique is the lack of clarity regarding its precise effects on neural activity. Here, we examined the effects of TMS intensity and frequency on concurrently recorded blood-oxygen-level-dependent (BOLD) signals at the site of stimulation. In two experiments, we delivered TMS to the dorsolateral prefrontal cortex in human subjects of both sexes. In Experiment 1, we delivered a series of pulses at high (100% of motor threshold) or low (50% of motor threshold) intensity, whereas, in Experiment 2, we always used high intensity but delivered stimulation at four different frequencies (5, 8.33, 12.5, and 25 Hz). We found that the TMS intensity and frequency could be reliably decoded using multivariate analysis techniques even though TMS had no effect on the overall BOLD activity at the site of stimulation in either experiment. These results provide important insight into the mechanisms through which TMS influences neural activity.

Action information contributes to metacognitive decision-making.

Metacognitive abilities allow us to adjust ongoing behavior and modify future decisions in the absence of external feedback. Although metacognition is critical in many daily life settings, it remains unclear what information is actually being monitored and what kind of information is being used for metacognitive decisions. In the present study, we investigated whether response information connected to perceptual events contribute to metacognitive decision-making. Therefore, we recorded EEG signals during a perceptual color discrimination task while participants were asked to provide an estimate about the quality of their decision on each trial. Critically, the moment participants provided their confidence judgments varied across conditions, thereby changing the amount of action information (e.g., response competition or response fluency) available for metacognitive decisions. Results from three experiments demonstrate that metacognitive performance improved when first-order action information was available at the moment metacognitive decisions about the perceptual task had to be provided. This behavioral effect was accompanied by enhanced functional connectivity (beta phase synchrony) between motor areas and prefrontal regions, exclusively observed during metacognitive decision-making. Our findings demonstrate that action information contributes to metacognitive decision-making, thereby painting a picture of metacognition as a process that integrates sensory evidence and information about our interactions with the world.

Competitive Frontoparietal Interactions Mediate Implicit Inferences.

Frequent experience with regularities in our environment allows us to use predictive information to guide our decision process. However, contingencies in our environment are not always explicitly present and sometimes need to be inferred. Heretofore, it remained unknown how predictive information guides decision-making when explicit knowledge is absent and how the brain shapes such implicit inferences. In the present experiment, 17 human participants (9 females) performed a discrimination task in which a target stimulus was preceded by a predictive cue. Critically, participants had no explicit knowledge that some of the cues signaled an upcoming target, allowing us to investigate how implicit inferences emerge and guide decision-making. Despite unawareness of the cue-target contingencies, participants were able to use implicit information to improve performance. Concurrent EEG recordings demonstrate that implicit inferences rely upon interactions between internally and externally oriented networks, whereby prefrontal regions inhibit parietal cortex under internal implicit control.SIGNIFICANCE STATEMENT Regularities in our environment can guide our behavior providing information about upcoming events. Interestingly, such predictive information does not need to be explicitly represented to effectively guide our decision process. Here, we show how the brain engages in such real-world "data mining" and how implicit inferences emerge. We used a contingency cueing task and demonstrated that implicit inferences influenced responses to subsequent targets despite a lack of awareness of cue-target contingencies. Further, we show that these implicit inferences emerge through interactions between internally and externally oriented neural networks. The current results highlight the importance of prefrontal processes in transforming external events into predictive internalized models of the world.

Sure I'm Sure: Prefrontal Oscillations Support Metacognitive Monitoring of Decision Making.

Successful decision making critically involves metacognitive processes such as monitoring and control of our decision process. Metacognition enables agents to modify ongoing behavior adaptively and determine what to do next in situations in which external feedback is not (immediately) available. Despite the importance of metacognition for many aspects of life, little is known about how our metacognitive system operates or about what kind of information is used for metacognitive (second-order) judgments. In particular, it remains an open question whether metacognitive judgments are based on the same information as first-order decisions. Here, we investigated the relationship between metacognitive performance and first-order task performance by recording EEG signals while participants were asked to make a "diagnosis" after seeing a sample of fictitious patient data (a complex pattern of colored moving dots of different sizes). To assess metacognitive performance, participants provided an estimate about the quality of their diagnosis on each trial. Results demonstrate that the information that contributes to first-order decisions differs from the information that supports metacognitive judgments. Further, time-frequency analyses of EEG signals reveal that metacognitive performance is associated specifically with prefrontal theta-band activity. Together, our findings are consistent with a hierarchical model of metacognition and suggest a crucial role for prefrontal oscillations in metacognitive performance. SIGNIFICANCE STATEMENT: Monitoring and control of our decision process (metacognition) is a crucial aspect of adaptive decision making. Crucially, metacognitive skills enable us to adjust ongoing behavior and determine future decision making when immediate feedback is not available. In the present study, we constructed a "diagnosis task" that allowed us to assess in what way first-order task performance and metacognition are related to each other. Results demonstrate that the contribution of sensory evidence (size, color, and motion direction) differs between first- and second-order decision making. Further, our results indicate that metacognitive performance specifically is orchestrated by means of prefrontal theta oscillations. Together, our findings suggest a hierarchical model of metacognition.

Conflict in the kitchen: Contextual modulation of responsiveness to affordances.

Recently, human behavior has been considered the product of continuous interactions between perception, cognition and action in which "affordances" (action possibilities the environment has to offer) play an important role. Converging evidence suggests that multiple action possibilities simultaneously compete for further processing, while external and internal factors (e.g., incoming sensory information, predictions) bias this competition. In the present study we used a stop-task to investigate whether context is able to modulate the strength of the responsiveness to affordances. We therefore placed participants in an actual kitchen and workshop during electroencephalographic recordings. A faster response to context congruent objects demonstrated that the direct surrounding is able to affect responsiveness to affordances. In addition, when responses needed to be withheld, context congruent objects evoked greater response conflict as indicated by an enhanced N2 Event Related Potential (ERP) component.

Opposing dorsal/ventral stream dynamics during figure-ground segregation.

The visual system has been commonly subdivided into two segregated visual processing streams: The dorsal pathway processes mainly spatial information, and the ventral pathway specializes in object perception. Recent findings, however, indicate that different forms of interaction (cross-talk) exist between the dorsal and the ventral stream. Here, we used TMS and concurrent EEG recordings to explore these interactions between the dorsal and ventral stream during figure-ground segregation. In two separate experiments, we used repetitive TMS and single-pulse TMS to disrupt processing in the dorsal (V5/HMT⁺) and the ventral (lateral occipital area) stream during a motion-defined figure discrimination task. We presented stimuli that made it possible to differentiate between relatively low-level (figure boundary detection) from higher-level (surface segregation) processing steps during figure-ground segregation. Results show that disruption of V5/HMT⁺ impaired performance related to surface segregation; this effect was mainly found when V5/HMT⁺ was perturbed in an early time window (100 msec) after stimulus presentation. Surprisingly, disruption of the lateral occipital area resulted in increased performance scores and enhanced neural correlates of surface segregation. This facilitatory effect was also mainly found in an early time window (100 msec) after stimulus presentation. These results suggest a "push-pull" interaction in which dorsal and ventral extrastriate areas are being recruited or inhibited depending on stimulus category and task demands.

Biasing neural network dynamics using non-invasive brain stimulation.

Recently, non-invasive brain stimulation (NBS) has been discovered as a tool to improve human performance on a wide variety of tasks. Although these observations are highly intriguing, the underlying mechanisms of such enhancements are still poorly understood. Here, we argue that in order to advance our understanding of these mechanisms it is necessary to focus on intrinsic network dynamics in the brain. Taking into account well-known network dynamics, increased excitation in one particular network or brain region may necessarily lead to inhibition of an opposing network (and vice versa). As a consequence, observed behavioral improvements due to NBS may emerge from a shift in the balance between (competing) neural networks in the brain, implicating that behavioral enhancement due to stimulation most likely comes with a cost or side effect. We conclude that more elaborate experimental designs are essential for a better understanding of the relationship between network interactions and the behavioral effects of NBS.

Confuse your illusion: feedback to early visual cortex contributes to perceptual completion.

A striking example of the constructive nature of visual perception is how the human visual system completes contours of occluded objects. To date, it is unclear whether perceptual completion emerges during early stages of visual processing or whether higher-level mechanisms are necessary. To answer this question, we used transcranial magnetic stimulation to disrupt signaling in V1/V2 and in the lateral occipital (LO) area at different moments in time while participants performed a discrimination task involving a Kanizsa-type illusory figure. Results show that both V1/V2 and higher-level visual area LO are critically involved in perceptual completion. However, these areas seem to be involved in an inverse hierarchical fashion, in which the critical time window for V1/V2 follows that for LO. These results are in line with the growing evidence that feedback to V1/V2 contributes to perceptual completion.

Two critical periods in early visual cortex during figure-ground segregation.

The ability to distinguish a figure from its background is crucial for visual perception. To date, it remains unresolved where and how in the visual system different stages of figure-ground segregation emerge. Neural correlates of figure border detection have consistently been found in early visual cortex (V1/V2). However, areas V1/V2 have also been frequently associated with later stages of figure-ground segregation (such as border ownership or surface segregation). To causally link activity in early visual cortex to different stages of figure-ground segregation, we briefly disrupted activity in areas V1/V2 at various moments in time using transcranial magnetic stimulation (TMS). Prior to stimulation we presented stimuli that made it possible to differentiate between figure border detection and surface segregation. We concurrently recorded electroencephalographic (EEG) signals to examine how neural correlates of figure-ground segregation were affected by TMS. Results show that disruption of V1/V2 in an early time window (96-119 msec) affected detection of figure stimuli and affected neural correlates of figure border detection, border ownership, and surface segregation. TMS applied in a relatively late time window (236-259 msec) selectively deteriorated performance associated with surface segregation. We conclude that areas V1/V2 are not only essential in an early stage of figure-ground segregation when figure borders are detected, but subsequently causally contribute to more sophisticated stages of figure-ground segregation such as surface segregation.

The flexible nature of unconscious cognition.

The cognitive signature of unconscious processes is hotly debated recently. Generally, consciousness is thought to mediate flexible, adaptive and goal-directed behavior, but in the last decade unconscious processing has rapidly gained ground on traditional conscious territory. In this study we demonstrate that the scope and impact of unconscious information on behavior and brain activity can be modulated dynamically on a trial-by-trial basis. Participants performed a Go/No-Go experiment in which an unconscious (masked) stimulus preceding a conscious target could be associated with either a Go or No-Go response. Importantly, the mapping of stimuli onto these actions varied on a trial-by-trial basis, preventing the formation of stable associations and hence the possibility that unconscious stimuli automatically activate these control actions. By eliminating stimulus-response associations established through practice we demonstrate that unconscious information can be processed in a flexible and adaptive manner. In this experiment we show that the same unconscious stimulus can have a substantially different effect on behavior and (prefrontal) brain activity depending on the rapidly changing task context in which it is presented. This work suggests that unconscious information processing shares many sophisticated characteristics (including flexibility and context-specificity) with its conscious counterpart.

Magnetic stimulation of the dorsolateral prefrontal cortex dissociates fragile visual short-term memory from visual working memory.

To guide our behavior in successful ways, we often need to rely on information that is no longer in view, but maintained in visual short-term memory (VSTM). While VSTM is usually broken down into iconic memory (brief and high-capacity store) and visual working memory (sustained, yet limited-capacity store), recent studies have suggested the existence of an additional and intermediate form of VSTM that depends on activity in extrastriate cortex. In previous work, we have shown that this fragile form of VSTM can be dissociated from iconic memory. In the present study, we provide evidence that fragile VSTM is different from visual working memory as magnetic stimulation of the right dorsolateral prefrontal cortex (DLPFC) disrupts visual working memory, while leaving fragile VSTM intact. In addition, we observed that people with high DLPFC activity had superior working memory capacity compared to people with low DLPFC activity, and only people with high DLPFC activity really showed a reduction in working memory capacity in response to magnetic stimulation. Altogether, this study shows that VSTM consists of three stages that have clearly different characteristics and rely on different neural structures. On the methodological side, we show that it is possible to predict individual susceptibility to magnetic stimulation based on functional MRI activity.