Effects of Experiencing CS-US Pairings on Instructed Fear Reversal.

Fear learning allows us to identify and anticipate aversive events and adapt our behavior accordingly. This is often thought to rely on associative learning mechanisms where an initially neutral conditioned stimulus (CS) is repeatedly paired with an aversive unconditioned stimulus (US), eventually leading to the CS also being perceived as aversive and threatening. Importantly, however, humans also show verbal fear learning. Namely, they have the ability to change their responses to stimuli rapidly through verbal instructions about CS-US pairings. Past research on the link between experience-based and verbal fear learning indicated that verbal instructions about a reversal of CS-US pairings can fully override the effects of previously experienced CS-US pairings, as measured through fear ratings, skin conductance, and fear-potentiated startle. However, it remains an open question whether such instructions can also annul learned CS representations in the brain. Here, we used a fear reversal paradigm (female and male participants) in conjunction with representational similarity analysis of fMRI data to test whether verbal instructions fully override the effects of experienced CS-US pairings in fear-related brain regions or not. Previous research suggests that only the right amygdala should show lingering representations of previously experienced threat ("pavlovian trace"). Unexpectedly, we found evidence for the residual effect of prior CS-US experience to be much more widespread than anticipated, in the amygdala but also cortical regions like the dorsal anterior cingulate or dorsolateral prefrontal cortex. This finding shines a new light on the interaction of different fear learning mechanisms, at times with unexpected consequences.SIGNIFICANCE STATEMENT Humans are able to learn about aversive stimuli both from experience (i.e., repeated pairings of conditioned stimulus (CS) and unconditioned stimulus (US; pavlovian conditioning), and from verbal instructions about stimulus pairings. Understanding how experience-based and verbal learning processes interact is key for understanding the cognitive and neural underpinnings of fear learning. We tested whether prior aversive experiences (CS-US pairings) affected subsequent verbal learning, searching for lingering threat signals after verbal instructions reversed a CS from being threatening to being safe. While past research suggested such threat signals can only be found in the amygdala, we found evidence to be much more widespread, including the medial and lateral PFC. This highlights how experience-based and verbal learning processes interact to support adaptive behavior.

Associative Visuomotor Learning Using Transcranial Magnetic Stimulation Induces Stimulus-Response Interference.

Classical conditioning states that the systematic co-occurrence of a neutral stimulus with an unconditioned stimulus can cause the neutral stimulus to, over time, evoke the same response as the unconditioned stimulus. On a neural level, Hebbian learning suggests that this type of learning occurs through changes in synaptic plasticity when two neurons are simultaneously active, resulting in increased connectivity between them. Inspired by associative learning theories, we here investigated whether the mere co-activation of visual stimuli and stimulation of the primary motor cortex using TMS would result in stimulus-response associations that can impact future behavior. During a learning phase, we repeatedly paired the presentation of a specific color (but not other colors) with a TMS pulse over the motor cortex. Next, participants performed a two-alternative forced-choice task where they had to categorize simple shapes and we studied whether the shapes' task-irrelevant color (and its potentially associated involuntary motor activity) affected the required motor response. Participants showed more errors on incongruent trials for stimuli that were previously paired with high intensity TMS pulses, but only when tested on the same day. Using a drift diffusion model for conflict tasks, we further demonstrate that this interference occurred early, and gradually increased as a function of associated TMS intensity. Taken together, our findings show that the human brain can learn stimulus-response associations using externally induced motor cortex stimulation. Although we were inspired by the Hebbian learning literature, future studies should investigate whether Hebbian or other learning processes were also what brought about this effect.

Reduced Primacy Bias in Autism during Early Sensory Processing.

Recent theories of autism propose that a core deficit in autism would be a less context-sensitive weighting of prediction errors. There is also first support for this hypothesis on an early sensory level. However, an open question is whether this decreased context sensitivity is caused by faster updating of one's model of the world (i.e., higher weighting of new information), proposed by predictive coding theories, or slower model updating. Here, we differentiated between these two hypotheses by investigating how first impressions shape the mismatch negativity (MMN), reflecting early sensory prediction error processing. An autism and matched control group of human adults (both n = 27, 8 female) were compared on the multi-timescale MMN paradigm, in which tones were presented that were either standard (frequently occurring) or deviant (rare), and these roles reversed every block. A well-replicated observation is that the initial model (i.e., the standard and deviant sound in the first block) influences MMN amplitudes in later blocks. If autism is characterized by faster model updating, and thus a smaller primacy bias, we hypothesized (and demonstrate using a simple reinforcement learning model) that their MMN amplitudes should be less influenced by the initial context. In line with this hypothesis, we found that MMN responses in the autism group did not differ between the initial deviant and initial standard sounds as they did in the control group. These findings are consistent with the idea that autism is characterized by faster model updating during early sensory processing, as proposed by predictive coding accounts of autism.SIGNIFICANCE STATEMENT Recent theories of autism propose that a core deficit in autism is that they are faster to update their models of the world based on new sensory information. Here, we tested this hypothesis by investigating how first impressions shape brain responses during early sensory processing, and hypothesized that individuals with autism would be less influenced by these first impressions. In line with earlier studies, our results show that early sensory processing was influenced by first impressions in a control group. However, this was not the case in an autism group. This suggests that individuals with autism are faster to abandon their initial model, and is consistent with the proposal that they are faster to update their models of the world.

Adaptive coding of stimulus information in human frontoparietal cortex during visual classification.

The neural mechanisms of how frontal and parietal brain regions support flexible adaptation of behavior remain poorly understood. Here, we used functional magnetic resonance imaging (fMRI) and representational similarity analysis (RSA) to investigate frontoparietal representations of stimulus information during visual classification under varying task demands. Based on prior research, we predicted that increasing perceptual task difficulty should lead to adaptive changes in stimulus coding: task-relevant category information should be stronger, while task-irrelevant exemplar-level stimulus information should become weaker, reflecting a focus on the behaviorally relevant category information. Counter to our expectations, however, we found no evidence for adaptive changes in category coding. We did find weakened coding at the exemplar-level within categories however, demonstrating that task-irrelevant information is de-emphasized in frontoparietal cortex. These findings reveal adaptive coding of stimulus information at the exemplar-level, highlighting how frontoparietal regions might support behavior even under challenging conditions.

The impact of free will beliefs on implicit learning.

A growing number of studies demonstrate that belief in free will (FWB) is dynamic, and can be reduced experimentally. Most of these studies assume that doing so has beneficial effects on behavior, as FWBs are thought to subdue unwanted automatic processes (e.g. racial stereotypes). However, relying on automatic processes can sometimes be advantageous, for instance during implicit learning (e.g. detecting and exploiting statistical regularities in the environment). In this registered report, we tested whether experimentally reducing FWBs positively affected implicit motor learning. We hypothesized that reducing FWBs would lead to both faster and stronger implicit learning, as measured using the alternating serial reaction time (ASRT) task. While we did show a manipulation effect on free will beliefs, there was no detectable effect on implicit learning processes. This finding adds to the growing body of evidence that free will belief manipulations do not meaningfully affect downstream behavior.

Manipulating Belief in Free Will and Its Downstream Consequences: A Meta-Analysis.

Ever since some scientists and popular media put forward the idea that free will is an illusion, the question has risen what would happen if people stopped believing in free will. Psychological research has investigated this question by testing the consequences of experimentally weakening people's free will beliefs. The results of these investigations have been mixed, with successful experiments and unsuccessful replications. This raises two fundamental questions: Can free will beliefs be manipulated, and do such manipulations have downstream consequences? In a meta-analysis including 145 experiments (95 unpublished), we show that exposing individuals to anti-free will manipulations decreases belief in free will and increases belief in determinism. However, we could not find evidence for downstream consequences. Our findings have important theoretical implications for research on free will beliefs and contribute to the discussion of whether reducing people's belief in free will has societal consequences.

Manipulating free will beliefs using online video games.

Research in social psychology and experimental philosophy has investigated lay people's free will beliefs (FWB). Using different approaches (i.e. experimental manipulations and vignette studies), they investigated how FWB relate to other concepts, and whether changing FWB has an impact on downstream processes such as social behavior. However, both approaches have shortcomings. While experimental manipulations used in social psychology suffer from demand effects, vignettes used in experimental philosophy are often highly abstract. Across two pre-registered studies, we developed a new approach by merging them in an online video game setting. Using this novel, experience-based FWB manipulation, we found that decreasing FWB impacted variables such as perceived control and responsibility in both studies. While the experience-based manipulation influenced participants' beliefs in free will within the context of the experience ("Within the context of the scenario, would the agent believe in free will?") in the first study, this manipulation effect did not transfer to participants' general FWB ("Do you believe in free will?") in the second study. Overall, our findings suggest a way forward in studying laypeople's beliefs in free will.

Does belief in free will influence biological motion perception?

Previous research suggests that belief in free will correlates with intentionality attribution. However, whether belief in free will is also related to more basic social processes is unknown. Based on evidence that biological motion contains intentionality cues that observers spontaneously extract, we investigate whether people who believe more in free will, or in related constructs, such as dualism and determinism, would be better at picking up such cues and therefore at detecting biological agents hidden in noise, or would be more inclined to detect intentionality cues and therefore to detect biological agents even when there are none. Signal detection theory was used to measure participants' ability to detect biological motion from scrambled background noise (d') and their response bias (c) in doing so. In two experiments, we found that belief in determinism and belief in dualism, but not belief in free will, were associated with biological motion perception. However, no causal effect was found when experimentally manipulating free will-related beliefs. In sum, our results show that biological motion perception, a low-level social process, is related to high-level beliefs about dualism and determinism.

Metacognitive Awareness of Difficulty in Action Selection: The Role of the Cingulo-opercular Network.

The question whether and how we are able to monitor our own cognitive states (metacognition) has been a matter of debate for decades. Do we have direct access to our cognitive processes, or can we only infer them indirectly based on their consequences? In the current study, we wanted to investigate the brain circuits that underlie the metacognitive experience of fluency in action selection. To manipulate action-selection fluency, we used a subliminal response priming paradigm. On each trial, both male and female human participants additionally engaged in the metacognitive process of rating how hard they felt it was to respond to the target stimulus. Despite having no conscious awareness of the prime, results showed that participants rated incompatible trials (during which subliminal primes interfered with the required response) to be more difficult than compatible trials (where primes facilitated the required response), reflecting metacognitive awareness of difficulty. This increased sense of subjective difficulty was mirrored by increased activity in the rostral cingulate zone and the anterior insula, two regions that are functionally closely connected. Importantly, this reflected activations that were unique to subjective difficulty ratings and were not explained by RTs or prime-response compatibility. We interpret these findings in light of a possible grounding of the metacognitive judgment of fluency in action selection in interoceptive signals resulting from increased effort.

Neural oscillations track the maintenance and proceduralization of novel instructions.

Humans are capable of flexibly converting symbolic instructions into novel behaviors. Previous evidence and theoretical models suggest that the implementation of a novel instruction requires the reformatting of its declarative content into an action-oriented code optimized for the execution of the instructed behavior. While neuroimaging research focused on identifying the brain areas involved in such a process, the temporal and electrophysiological mechanisms remain poorly understood. These mechanisms, however, can provide information about the specific cognitive processes that characterize the proceduralization of information. In the present study, we recorded EEG activity while we asked participants to either simply maintain declaratively the content of novel S-R mappings or to proactively prepare for their implementation. By means of time-frequency analyses, we isolated the oscillatory features specific to the proceduralization of instructions. Implementation of the instructed mappings elicited stronger theta activity over frontal electrodes and suppression in mu and beta activity over central electrodes. On the contrary, activity in the alpha band, which has been shown to track the attentional deployment to task-relevant items, showed no differences between tasks. Together, these results support the idea that proceduralization of information is characterized by specific component processes such as orchestrating complex task settings and configuring the motor system that are not observed when instructions are held in a declarative format.

Frontoparietal action-oriented codes support novel instruction implementation.

A key aspect of human cognitive flexibility concerns the ability to convert complex symbolic instructions into novel behaviors. Previous research proposes that this transformation is supported by two neurocognitive states: an initial declarative maintenance of task knowledge, and an implementation state necessary for optimal task execution. Furthermore, current models predict a crucial role of frontal and parietal brain regions in this process. However, whether declarative and procedural signals independently contribute to implementation remains unknown. We report the results of an fMRI experiment in which participants executed novel instructed stimulus-response associations. We then used a pattern-tracking procedure to quantify the contribution of format-unique signals during instruction implementation. This revealed independent procedural and declarative representations of novel S-Rs in frontoparietal areas, prior to execution. Critically, the degree of procedural activation predicted subsequent behavioral performance. Altogether, our results suggest an important contribution of frontoparietal regions to the neural architecture that regulates cognitive flexibility.

Reward does not modulate corticospinal excitability in anticipation of a Stroop trial.

Action preparation is associated with a transient decrease of corticospinal excitability just before target onset. We have previously shown that the prospect of reward modulates preparatory corticospinal excitability in a Simon task. While the conflict in the Simon task strongly implicates the motor system, it is unknown whether reward prospect modulates preparatory corticospinal excitability in tasks that implicate the motor system less directly. To that effect, we examined reward-modulated preparatory corticospinal excitability in the Stroop task. We administered a rewarded cue-target delay paradigm using Stroop stimuli that afforded a left or right index finger response. Single-pulse transcranial magnetic stimulation was administered over the left primary motor cortex and electromyography was obtained from the right first dorsal interosseous muscle. In line with previous findings, there was a preparatory decrease in corticospinal excitability during the delay period. In contrast to our previous study using the Simon task, preparatory corticospinal excitability was not modulated by reward. Our results indicate that reward-modulated changes in the motor system depend on specific task-demands, possibly related to varying degrees of motor conflict.

Early Approach and Avoidance Tendencies can be Goal-Directed: Support from a Transcranial Magnetic Stimulation Study.

Dual-process models with a default-interventionist architecture explain early emotional action tendencies by a stimulus-driven process, and they allow goal-directed processes to intervene only in a later stage. An alternative dual-process model with a parallel-competitive architecture developed by Moors, Boddez, and De Houwer (Emotion Review, 9(4), 310-318, 2017), in contrast, explains early emotional action tendencies by a goal-directed process. This model proposes that stimulus-driven and goal-directed processes often operate in parallel and compete with each other, and that if they do compete, the goal-directed process often wins the competition. To examine these predictions, we set up a goal-directed process in an experimental group by rewarding participants for avoiding positive stimuli and for approaching negative stimuli and punishing them for the opposite behavior. We expected this process to compete with a potentially preexisting stimulus-driven process in which positive stimuli are associated with approach and negative stimuli with avoidance. We compared the elicited action tendencies of participants in this group with a control group in which only the stimulus-driven process could operate. Early approach and avoidance tendencies were assessed via motor evoked potentials (MEP) measured in the finger muscles previously trained to approach or to avoid stimuli after single-pulse transcranial magnetic stimulation (TMS) delivered at 400 ms. Results confirmed that positive/negative stimuli led to stronger avoidance/approach tendencies in the experimental group but not to approach/avoidance tendencies in the control group. This suggests that goal-directed processes are indeed able to determine relatively early emotional action tendencies, but it does not show that goal-directed process can defeat stimulus-driven processes.

Representing Multiple Observed Actions in the Motor System.

There is now converging evidence that others' actions are represented in the motor system. However, social cognition requires us to represent not only the actions but also the interactions of others. To do so, it is imperative that the motor system can represent multiple observed actions. The current fMRI study investigated whether this is possible by measuring brain activity from 29 participants while they observed 2 right hands performing sign language gestures. Three key results were obtained. First, brain activity in the premotor and parietal motor cortex was stronger when 2 hands performed 2 different gestures than when 1 hand performed a single gesture. Second, both individual observed gestures could be decoded from brain activity in the same 2 regions. Third, observing 2 different gestures compared with 2 identical gestures activated brain areas related to motor conflict, and this activity was correlated with parietal motor activity. Together, these results show that the motor system is able to represent multiple observed actions, and as such reveal a potential mechanism by which third-party social encounters could be processed in the brain.

The influence of threat on perceived spatial distance to out-group members.

A classic example of discriminatory behavior is keeping spatial distance from an out-group member. To explain this social behavior, the literature offers two alternative theoretical options that we label as the "threat hypothesis" and the "shared-experience hypothesis". The former relies on studies showing that out-group members create a sense of alertness. Consequently, potentially threatening out-group members are represented as spatially close allowing the prevention of costly errors. The latter hypothesis suggests that the observation of out-group members reduces the sharing of somatosensory experiences and, thus, increases the perceived physical distance between oneself and others. In the present paper, we pitted the two hypotheses against each other. In Experiment 1, Caucasian participants expressed multiple implicit "Near/Far" spatial categorization judgments from a Black-African Avatar and a White-Caucasian Avatar located in a 3D environment. Results indicate that the Black-African Avatar was categorized as closer to oneself, as compared with the White-Caucasian Avatar, providing support for "the threat hypothesis". In Experiment 2, we tested to which degree perceived threat contributes to this categorization bias by manipulating the avatar's perceived threat orthogonally to group membership. The results indicate that irrespective of group membership, threatening avatars were categorized as being closer to oneself as compared with no threatening avatars. This suggests that provided information about a person and not the mere group membership influences perceived distance to the person.

Measuring spontaneous mentalizing with a ball detection task: putting the attention-check hypothesis by Phillips and colleagues (2015) to the test.

Theory of Mind (ToM) or mentalizing refers to the ability to attribute mental states (such as desires, beliefs or intentions) to oneself or others. ToM has been argued to operate in an explicit and an implicit or a spontaneous way. In their influential paper, Kovács et al. (Science 330:1830-1834, 2010) introduced an adapted false belief task-a ball detection task-for the measurement of spontaneous ToM. Since then, several studies have successfully used versions of this paradigm to investigate spontaneous ToM. This paradigm has, however, been criticized by Phillips et al. (Psychol Sci 26(9):1353-1367, 2015), who argue that the effects are fully explained by timing artifacts in the paradigm, namely differences in timing of the attention check. The main objective of the current study is to test this attention-check hypothesis. An additional aim was to relate the findings to autism spectrum disorder (ASD) symptomatology in our neurotypical sample, as ASD has been linked to deficits in spontaneous mentalizing. We applied an adjusted version of the paradigm in which the timings for all conditions are equalized, ruling out any potential timing confounds. We found significant main effects of own and agent beliefs on reaction times. Additionally, we found a significant 'ToM-effect': When participants believe the ball is absent, they detect the ball faster if the agent believes the ball would be present rather than absent, which refers to the original effect in the paper of Kovács et al. (2010), taken as evidence for spontaneous ToM and which was contested by Phillips et al. (2015). Our findings cannot be explained by the attention-check hypothesis. Effects could not be associated with ASD symptoms in our neurotypical sample, warranting further investigation on the link between spontaneous mentalizing and ASD.

Belief in free will affects causal attributions when judging others' behavior.

Free will is a cornerstone of our society, and psychological research demonstrates that questioning its existence impacts social behavior. In six studies, we tested whether believing in free will is related to the correspondence bias, which reflects people's automatic tendency to overestimate the influence of internal as compared to external factors when interpreting others' behavior. All studies demonstrate a positive relationship between the strength of the belief in free will and the correspondence bias. Moreover, in two experimental studies, we showed that weakening participants' belief in free will leads to a reduction of the correspondence bias. Finally, the last study demonstrates that believing in free will predicts prescribed punishment and reward behavior, and that this relation is mediated by the correspondence bias. Overall, these studies show that believing in free will impacts fundamental social-cognitive processes that are involved in the understanding of others' behavior.

Defining the neural correlates of spontaneous theory of mind (ToM): An fMRI multi-study investigation.

There is a major debate in the theory of mind (ToM) field, concerning whether spontaneous and explicit ToM are based on the same or two distinct cognitive systems. While extensive research on the neural correlates of explicit ToM has demonstrated involvement of the temporo-parietal junction (TPJ) and the medial prefrontal cortex (mPFC), few studies investigated spontaneous ToM, leaving some open questions. Here, we implemented a multi-study approach by pooling data from three fMRI studies to obtain a larger sample to increase power and sensitivity to better define the neurocognitive mechanisms underlying spontaneous ToM. Participants watched videos in which an agent acquires a true or false belief about the location of a ball. Thus, the belief of the agent and that of the participant could either match or differ. Importantly, participants were never asked to consider the belief of the agent and were only instructed to press a button when they detected the presence of the ball after an occluder fell at the end of each video. By analysing the blood-oxygen level dependent signal during the belief formation phase for false versus true beliefs, we found a cluster of activation in the right, and to a lesser extent, left posterior parietal cortex spanning the TPJ, but no mPFC activation. Region of interest (ROI) analysis on bilateral TPJ and mPFC confirmed these results and added evidence to the asymmetry in laterality of the TPJ in spontaneous ToM. Interestingly, the whole brain analysis, supported by an overlap with brain maps, revealed maximum activation in areas involved in visuospatial working memory and attention switching functions, such as the supramarginal gyrus, the middle temporal gyrus, and the inferior frontal gyrus. By contrast, evidence for the presence of brain-behaviour correlations was mixed and there was no evidence for functional connectivity between the TPJ and mPFC. Taken together, these findings help clarifying the brain system supporting spontaneous ToM.

The neural representation of mental beliefs held by two agents.

Neuroimaging research has demonstrated that mentalizing about false beliefs held by other people recruits the temporo-parietal junction (TPJ). However, earlier work was limited to a single agent that held a false belief. We investigated the effect of two agents that held similar or mixed false and/or true beliefs. Participants saw animated stories with two smurfs holding true or false beliefs (Story phase). At the end of each trial, they were requested to take the perspective of the self or one of the smurfs (Question phase). We predicted that an increasing number of smurfs holding a false belief would increase activation in the TPJ when participants have to report the belief of the smurf, because the incongruent belief should have a stronger influence if it is held by two compared with one agent. This prediction was confirmed as activation in the TPJ during the Story and Question phase increased when more smurfs held a false belief. Taking the perspective of the self led to stronger activation of the TPJ in the two conditions that involved a true belief and weakest activation in the condition of two false beliefs. These data suggest that activation in TPJ depends on the perspective participants take, and that the number of agents holding a false belief influences activation in the TPJ only when taking the agent's perspective.

The Role of the Temporoparietal Junction in Self-Other Distinction.

Being able to discriminate between what originates from ourselves and what originates from others is critical for efficient interactions with our social environment. However, it remains an open question whether self-other distinction is a domain-general mechanism that is involved in various social-cognitive functions or whether specific 'self-other distinction mechanisms' exist for each of these functions. On the neural level, there is evidence that self-other distinction is related to a specific brain region at the border of the superior temporal and inferior parietal cortex, the temporoparietal junction (TPJ). Demonstrating that the TPJ plays a role in social processes that require self-other distinction would support the idea of a domain-general mechanism of self-other distinction. In the present paper, we review evidence coming from clinical observations, neuroimaging experiments and a meta-analysis indicating the involvement of the TPJ in various cognitive operations requiring self-other distinction. At the perceptual level, we discuss the human ability to identify one's own body and to distinguish it from others. At the action level, we review research on the human ability to experience agency and the control of imitative response tendencies. Finally, at the mental-state level, we discuss the ability to attribute mental states to others. Based on this integrative review, we suggest that the TPJ, and in particular its dorsal part, supports a domain general ability to enhance task-relevant representations when self-related and other-related representations are in conflict. Finally, this conception allows us to propose a unifying architecture for the emergence of numerous socio-cognitive abilities.