Sleep consolidates stimulus-response learning.

Performing a motor response to a sensory stimulus creates a memory trace whose behavioral correlates are classically investigated in terms of repetition priming effects. Such stimulus-response learning entails two types of associations that are partly independent: (1) an association between the stimulus and the motor response and (2) an association between the stimulus and the classification task in which it is encountered. Here, we tested whether sleep supports long-lasting stimulus-response learning on a task requiring participants (1) for establishing stimulus-classification associations to classify presented objects along two different dimensions ("size" and "mechanical") and (2) as motor response (action) to respond with either the left or right index finger. Moreover, we examined whether strengthening of stimulus-classification associations is preferentially linked to nonrapid eye movement (non-REM) sleep and strengthening of stimulus-action associations to REM sleep. We tested 48 healthy volunteers in a between-subjects design comparing postlearning retention periods of nighttime sleep versus daytime wakefulness. At postretention testing, we found that sleep supports consolidation of both stimulus-action and stimulus-classification associations, as indicated by increased reaction times in "switch conditions"; that is, when, at test, the acutely instructed classification task and/or correct motor response for a given stimulus differed from that during original learning. Polysomnographic recordings revealed that both kinds of associations were correlated with non-REM spindle activity. Our results do not support the view of differential roles for non-REM and REM sleep in the consolidation of stimulus-classification and stimulus-action associations, respectively.

Human Brain Ages With Hierarchy-Selective Attenuation of Prediction Errors.

From the perspective of predictive coding, our brain embodies a hierarchical generative model to realize perception, which proactively predicts the statistical structure of sensory inputs. How are these predictive processes modified as we age? Recent research suggested that aging leads to decreased weighting of sensory inputs and increased reliance on predictions. Here we investigated whether this age-related shift from sensorium to predictions occurs at all levels of hierarchical message passing. We recorded the electroencephalography responses with an auditory local-global paradigm in a cohort of 108 healthy participants from 3 groups: seniors, adults, and adolescents. The detection of local deviancy seems largely preserved in older individuals at earlier latency (including the mismatch negativity followed by the P3a but not the reorienting negativity). In contrast, the detection of global deviancy is clearly compromised in older individuals, as they showed worse task performance and attenuated P3b. Our findings demonstrate that older brains show little decline in sensory (i.e., first-order) prediction errors but significant diminution in contextual (i.e., second-order) prediction errors. Age-related deficient maintenance of auditory information in working memory might affect whether and how lower-level prediction errors propagate to the higher level.

Visual Predictions Operate on Different Timescales.

Humans live in a volatile environment, subject to changes occurring at different timescales. The ability to adjust internal predictions accordingly is critical for perception and action. We studied this ability with two EEG experiments in which participants were presented with sequences of four Gabor patches, simulating a rotation, and instructed to respond to the last stimulus (target) to indicate whether or not it continued the direction of the first three stimuli. Each experiment included a short-term learning phase in which the probabilities of these two options were very different (p = .2 vs. p = .8, Rules A and B, respectively), followed by a neutral test phase in which both probabilities were equal. In addition, in one of the experiments, prior to the short-term phase, participants performed a much longer long-term learning phase where the relative probabilities of the rules predicting targets were opposite to those of the short-term phase. Analyses of the RTs and P3 amplitudes showed that, in the neutral test phase, participants initially predicted targets according to the probabilities learned in the short-term phase. However, whereas participants not pre-exposed to the long-term learning phase gradually adjusted their predictions to the neutral probabilities, for those who performed the long-term phase, the short-term associations were spontaneously replaced by those learned in that phase. This indicates that the long-term associations remained intact whereas the short-term associations were learned, transiently used, and abandoned when the context changed. The spontaneous recovery suggests independent storage and control of long-term and short-term associations.

Execution-based and verbal code-based stimulus-response associations: proportion manipulations reveal conflict adaptation processes in item-specific priming.

Stimulus-response (S-R) associations consist of two independent components: Stimulus-classification (S-C) and stimulus-action (S-A) associations. Here, we examined whether these S-C and S-A associations were modulated by cognitive control operations. In two item-specific priming experiments, we systematically manipulated the proportion of trials in which item-specific S-C and/or S-A mappings repeated or switched between the single encoding (prime) and single retrieval (probe) instance of each stimulus (i.e., each stimulus appeared only twice). Thus, we assessed the influence of a list-level proportion switch manipulation on the strength of item-specific S-C and S-A associations. Participants responded slower and committed more errors when item-specific S-C or S-A mappings switched rather than repeated between prime and probe (i.e., S-C/S-A switch effects). S-C switch effects were larger when S-C repetitions rather than switches were frequent on the list-level. Similarly, S-A switch effects were modulated by S-A switch proportion. Most importantly, our findings rule out contingency learning and temporal learning as explanations of the observed results and point towards a conflict adaptation mechanism that selectively adapts the encoding and/or retrieval for each S-R component. Finally, we outline how cognitive control over S-R associations operates in the context of item-specific priming.

Defining stimulus representation in stimulus-response associations formed on the basis of task execution and verbal codes.

Responding to stimuli leads to the formation of stimulus-response (S-R) associations that allow stimuli to subsequently automatically trigger associated responses. A recent study has shown that S-R associations are established not only by active task execution, but also by the simultaneous presentation of stimuli and verbal codes denoting responses in the absence of own action [Pfeuffer et al. (Journal of Experimental Psychology: Human Perception and Performance 43:328-347, 2017)]. Here, we used an item-specific priming paradigm to investigate whether the stimulus part of S-R associations formed based on task execution and verbal codes is represented in abstract or specific format by examining whether S-R associations are retrieved for perceptually different forms of the same stimulus or not. Between the prime and probe instance of a stimulus, its format switched from image to word or vice versa. We found that, irrespective of whether stimuli were primed by task execution or verbal coding, performance was impaired when S-R mappings switched rather than repeated between the prime and probe instance of a stimulus. The finding that prime S-R mappings affected probe performance even when stimulus format switched indicates that stimuli were represented in abstract form in S-R association based on both task execution and verbal coding. Furthermore, we found no performance benefits for stimuli primed and probed in the same format rather than different formats, suggesting that stimuli were not additionally represented in specific format. Overall, our findings demonstrate the adaptability of automatized behaviors and indicate that abstract stimulus representations allow S-R associations to generalize across perceptually different stimulus formats.

Adaptive behaviour and feedback processing integrate experience and instruction in reinforcement learning.

In any non-deterministic environment, unexpected events can indicate true changes in the world (and require behavioural adaptation) or reflect chance occurrence (and must be discounted). Adaptive behaviour requires distinguishing these possibilities. We investigated how humans achieve this by integrating high-level information from instruction and experience. In a series of EEG experiments, instructions modulated the perceived informativeness of feedback: Participants performed a novel probabilistic reinforcement learning task, receiving instructions about reliability of feedback or volatility of the environment. Importantly, our designs de-confound informativeness from surprise, which typically co-vary. Behavioural results indicate that participants used instructions to adapt their behaviour faster to changes in the environment when instructions indicated that negative feedback was more informative, even if it was simultaneously less surprising. This study is the first to show that neural markers of feedback anticipation (stimulus-preceding negativity) and of feedback processing (feedback-related negativity; FRN) reflect informativeness of unexpected feedback. Meanwhile, changes in P3 amplitude indicated imminent adjustments in behaviour. Collectively, our findings provide new evidence that high-level information interacts with experience-driven learning in a flexible manner, enabling human learners to make informed decisions about whether to persevere or explore new options, a pivotal ability in our complex environment.

Temporal expectancies driven by self- and externally generated rhythms.

The dynamic attending theory proposes that rhythms entrain periodic fluctuations of attention which modulate the gain of sensory input. However, temporal expectancies can also be driven by the mere passage of time (foreperiod effect). It is currently unknown how these two types of temporal expectancy relate to each other, i.e. whether they work in parallel and have distinguishable neural signatures. The current research addresses this issue. Participants either tapped a 1Hz rhythm (active task) or were passively presented with the same rhythm using tactile stimulators (passive task). Based on this rhythm an auditory target was then presented early, in synchrony, or late. Behavioural results were in line with the dynamic attending theory as RTs were faster for in- compared to out-of-synchrony targets. Electrophysiological results suggested self-generated and externally induced rhythms to entrain neural oscillations in the delta frequency band. Auditory ERPs showed evidence of two distinct temporal expectancy processes. Both tasks demonstrated a pattern which followed a linear foreperiod effect. In the active task, however, we also observed an ERP effect consistent with the dynamic attending theory. This study shows that temporal expectancies generated by a rhythm and expectancy generated by the mere passage of time can work in parallel and sheds light on how these mechanisms are implemented in the brain.

Distinctive Representation of Mispredicted and Unpredicted Prediction Errors in Human Electroencephalography.

The predictive coding model of perception proposes that neuronal responses are modulated by the amount of sensory input that the internal prediction cannot account for (i.e., prediction error). However, there is little consensus on what constitutes nonpredicted stimuli. Conceptually, whereas mispredicted stimuli may induce both prediction error generated by prediction that is not perceived and prediction error generated by sensory input that is not anticipated, unpredicted stimuli involves no top-down, only bottom-up, propagation of information in the system. Here, we examined the possibility that the processing of mispredicted and unpredicted stimuli are dissociable at the neurophysiological level using human electroencephalography. We presented participants with sets of five tones in which the frequency of the fifth tones was predicted, mispredicted, or unpredicted. Participants were required to press a key when they detected a softer fifth tone to maintain their attention. We found that mispredicted and unpredicted stimuli are associated with different amount of cortical activity, probably reflecting differences in prediction error. Moreover, relative to predicted stimuli, the mispredicted prediction error manifested as neuronal enhancement and the unpredicted prediction error manifested as neuronal attenuation on the N1 event-related potential component. These results highlight the importance of differentiating between the two nonpredicted stimuli in theoretical work on predictive coding.

Agency alters perceptual decisions about action-outcomes.

Humans experience themselves as agents, capable of controlling their actions and the outcomes they generate (i.e., the sense of agency). Inferences of agency are not infallible. Research shows that we often attribute outcomes to our agency even though they are caused by another agent. Moreover, agents report the sensory events they generate to be less intense compared to the events that are generated externally. These effects have been assessed using highly suprathreshold stimuli and subjective measurements. Consequently, it remains unclear whether experiencing oneself as an agent lead to a decision criterion change and/or a sensitivity change. Here, we investigate this issue. Participants were told that their key presses generated an upward dot motion but that on 30 % of the trials the computer would take over and display a downward motion. The upward/downward dot motion was presented at participant's discrimination threshold. Participants were asked to indicate whether they (upward motion) or the computer (downward motion) generated the motion. This group of participants was compared with a 'no-agency' group who performed the same task except that subjects did not execute any actions to generate the dot motion. We observed that the agency group reported seeing more frequently the motion they expected to generate (i.e., upward motion) than the no-agency group. This suggests that agency distorts our experience of (allegedly) caused events by altering perceptual decision processes, so that, in ambiguous contexts, externally generated events are experienced as the outcomes of one's actions.

Reward activates stimulus-specific and task-dependent representations in visual association cortices.

Humans reliably learn which actions lead to rewards. One prominent question is how credit is assigned to environmental stimuli that are acted upon. Recent functional magnetic resonance imaging (fMRI) studies have provided evidence that representations of rewarded stimuli are activated upon reward delivery, providing possible eligibility traces for credit assignment. Our study sought evidence of postreward activation in sensory cortices satisfying two conditions of instrumental learning: postreward activity should reflect the stimulus category that preceded reward (stimulus specificity), and should occur only if the stimulus was acted on to obtain reward (task dependency). Our experiment implemented two tasks in the fMRI scanner. The first was a perceptual decision-making task on degraded face and house stimuli. Stimulus specificity was evident as rewards activated the sensory cortices associated with face versus house perception more strongly after face versus house decisions, respectively, particularly in the fusiform face area. Stimulus specificity was further evident in a psychophysiological interaction analysis wherein face-sensitive areas correlated with nucleus accumbens activity after face-decision rewards, whereas house-sensitive areas correlated with nucleus accumbens activity after house-decision rewards. The second task required participants to make an instructed response. The criterion of task dependency was fulfilled as rewards after face versus house responses activated the respective association cortices to a larger degree when faces and houses were relevant to the performed task. Our study is the first to show that postreward sensory cortex activity meets these two key criteria of credit assignment, and does so independently from bottom-up perceptual processing.

Repetition suppression comprises both attention-independent and attention-dependent processes.

Repetition suppression, a robust phenomenon of reduction in neural responses to stimulus repetition, is suggested to consist of a combination of bottom-up adaptation and top-down prediction effects. However, there is little consensus on how repetition suppression is related to attention in functional magnetic resonance imaging (fMRI) studies. It is probably because fMRI integrates neural activity related to adaptation and prediction effects, which are respectively attention-independent and attention-dependent. Here we orthogonally manipulated stimulus repetition and attention in a target detection task while participants' electroencephalography (EEG) was recorded. In Experiment 1, we found a significant repetition effect on N1 amplitude regardless of attention, whereas the repetition effect on P2 amplitude was attention-dependent. In Experiment 2 where the attentional manipulation was more stringent than that in Experiment 1, we replicated a significant repetition effect on N1 amplitude regardless of attention, whereas the repetition effect on P2 amplitude was eliminated. The results show that repetition suppression comprises both attention-independent and attention-dependent components.

Human perceptual decision making: disentangling task onset and stimulus onset.

The left dorsolateral prefrontal cortex (ldlPFC) has been highlighted as a key actor in human perceptual decision-making (PDM): It is theorized to support decision-formation independently of stimulus type or motor response. PDM studies however generally confound stimulus onset and task onset: when the to-be-recognized stimulus is presented, subjects know that a stimulus is shown and can set up processing resources-even when they do not know which stimulus is shown. We hypothesized that the ldlPFC might be involved in task preparation rather than decision-formation. To test this, we asked participants to report whether sequences of noisy images contained a face or a house within an experimental design that decorrelates stimulus and task onset. Decision-related processes should yield a sustained response during the task, whereas preparation-related areas should yield transient responses at its beginning. The results show that the brain activation pattern at task onset is strikingly similar to that observed in previous PDM studies. In particular, they contradict the idea that ldlPFC forms an abstract decision and suggest instead that its activation reflects preparation for the upcoming task. We further investigated the role of the fusiform face areas and parahippocampal place areas which are thought to be face and house detectors, respectively, that feed their signals to higher level decision areas. The response patterns within these areas suggest that this interpretation is unlikely and that the decisions about the presence of a face or a house in a noisy image might instead already be computed within these areas without requiring higher-order areas.

Dual process for intentional and reactive decisions.

Efficient cognitive decisions should be adjustable to incoming novel information. However, most current models of decision making have so far neglected any potential interaction between intentional and stimulus-driven decisions. We report here behavioral results and a new model on the interaction between a perceptual decision and non-predictable novel information. We asked participants to anticipate their response to an external stimulus and presented this stimulus with variable delay. Participants were clearly able to adjust their initial decision to the new stimulus if this latter appeared sufficiently early. To account for these results, we present a two-stage model in which two systems, an intentional and a stimulus-driven, interact only in the second stage. In the first stage of the model, the intentional and stimulus-driven processes race independently to reach a transition threshold between the two stages. The model can also account for results of a second experiment where a response bias is introduced. Our model is consistent with some physiological results that indicate that both parallel and interactive processing take place between intentional and stimulus-driven information. It emphasizes that in natural conditions, both types of processing are important and it helps pinpoint the transition between parallel and interactive processing.

The prediction of visual stimuli influences auditory loudness discrimination.

The brain combines information from different senses to improve performance on perceptual tasks. For instance, auditory processing is enhanced by the mere fact that a visual input is processed simultaneously. However, the sensory processing of one modality is itself subject to diverse influences. Namely, perceptual processing depends on the degree to which a stimulus is predicted. The present study investigated the extent to which the influence of one processing pathway on another pathway depends on whether or not the stimulation in this pathway is predicted. We used an action-effect paradigm to vary the match between incoming and predicted visual stimulation. Participants triggered a bimodal stimulus composed of a Gabor and a tone. The Gabor was either congruent or incongruent compared to an action-effect association that participants learned in an acquisition phase.We tested the influence of action-effect congruency on the loudness perception of the tone. We observed that an incongruent-task-irrelevant Gabor stimulus increases participant's sensitivity to loudness discrimination. An identical result was obtained for a second condition in which the visual stimulus was predicted by a cue instead of an action. Our results suggest that prediction error is a driving factor of the crossmodal interplay between vision and audition.

Give it a second try? The influence of feedback and performance in the decision of reattempting.

Feedback evaluation can affect behavioural continuation or discontinuation, and is essential for cognitive and motor skill learning. One critical factor that influences feedback evaluation is participants' internal estimation of self-performance. Previous research has shown that two event-related potential components, the Feedback-Related Negativity (FRN) and the P3, are related to feedback evaluation. In the present study, we used a time estimation task and EEG recordings to test the influence of feedback and performance on participants' decisions, and the sensitivity of the FRN and P3 components to those factors. In the experiment, participants were asked to reproduce the total duration of an intermittently presented visual stimulus. Feedback was given after every response, and participants had then to decide whether to retry the same trial and try to earn reward points, or to move on to the next trial. Results showed that both performance and feedback influenced participants' decision on whether to retry the ongoing trial. In line with previous studies, the FRN showed larger amplitude in response to negative than to positive feedback. Moreover, our results were also in agreement with previous works showing the relationship between the amplitude of the FRN and the size of feedback-related prediction error (PE), and provide further insight in how PE size influences participants' decisions on whether or not to retry a task. Specifically, we found that the larger the FRN, the more likely participants were to base their decision on their performance - choosing to retry the current trial after good performance or to move on to the next trial after poor performance, regardless of the feedback received. Conversely, the smaller the FRN, the more likely participants were to base their decision on the feedback received.

Advancements in brain-computer interfaces for the rehabilitation of unilateral spatial neglect: a concise review.

This short review examines recent advancements in neurotechnologies within the context of managing unilateral spatial neglect (USN), a common condition following stroke. Despite the success of brain-computer interfaces (BCIs) in restoring motor function, there is a notable absence of effective BCI devices for treating cerebral visual impairments, a prevalent consequence of brain lesions that significantly hinders rehabilitation. This review analyzes current non-invasive BCIs and technological solutions dedicated to cognitive rehabilitation, with a focus on visuo-attentional disorders. We emphasize the need for further research into the use of BCIs for managing cognitive impairments and propose a new potential solution for USN rehabilitation, by combining the clinical subtleties of this syndrome with the technological advancements made in the field of neurotechnologies.

The interaction between attention and motor prediction. An ERP study.

Performing a voluntary action involves the anticipation of the intended effect of that action. Interaction with the environment also requires the allocation of attention. However, the effects of attention upon motor predictive processes remain unclear. Here we use a novel paradigm to investigate attention and motor prediction orthogonally. In an acquisition phase, high and low tones were associated with left and right key presses. In the following test phase, tones were presented at random and participants attended to only one ear whilst ignoring tones presented in the unattended ear. In the test phase a tone could therefore be presented at the attended or unattended ear, as well as being congruent or incongruent with prior action-effect learning. We demonstrated early and late effects of attention as well as a later independent motor prediction effect with a larger P3a for incongruent tones. Interestingly, we demonstrated an intermediate interaction, showing an action-effect negativity (NAE) for tones which were unattended, whilst no motor prediction effect was found for attended tones. This interaction pattern suggests that attention and motor prediction are not opposing processes but can both operate to modulate prediction, providing valuable new insight into the relationship between attention and the effects of motor prediction.

Attenuation of auditory N1 results from identity-specific action-effect prediction.

The auditory N1 event-related potential has previously been observed to be attenuated for tones that are triggered by human actions. This attenuation is thought to be generated by motor prediction mechanisms and is considered to be important for agency attribution. The present study was designed to rigorously test the notion of action prediction-based sensory attenuation. Participants performed one of four voluntary actions on each trial, with each button associated with either predictable or unpredictable action effects. In addition, actions with each hand could result in action effects that were either congruent or incongruent with hand-specific prediction. We observed no significant differences in N1 amplitude between predictable and unpredictable tones. When contrasting action effects that were congruent or incongruent with hand-specific prediction, we observed significant attenuation for prediction-congruent compared to prediction-incongruent action-effects. These novel findings suggest that accurate action-effect prediction drives sensory attenuation of auditory stimuli. These findings have important implications for understanding the mechanisms of action-effect prediction and sensory attenuation, and may have clinical implications for studies investigating action awareness and agency in schizophrenia.

Imitating others' actions: transcranial magnetic stimulation of the parietal opercula reveals the processes underlying automatic imitation.

The human tendency to imitate gestures performed by conspecifics is automatic in nature. However, whether this automatic imitation can be considered as a true imitative phenomenon or only as a special instance of spatial compatibility is still being debated. New evidence suggests that automatic imitation, otherwise known as 'imitative compatibility', shall be considered as a phenomenon that operates independently from spatial compatibility. So far there are only a few investigations directly aimed at identifying the neural structures dedicated to this process. In the present study, we applied double-pulse transcranial magnetic stimulation (TMS) over the parietal opercula to further investigate the role of these regions in coding imitative compatibility. We found that a temporary disruption of parietal opercula caused the reduction of the imitative compatibility relative to the sham condition. In particular, the TMS interference with the parietal opercula's activity modulated the imitative compatibility but not the spatial compatibility, suggesting that these two processes are likely to be independent.

Durability of classification and action learning: differences revealed using ex-Gaussian distribution analysis.

It has been shown that in associative learning it is possible to disentangle the effects caused on behaviour by the associations between a stimulus and a classification (S-C) and the associations between a stimulus and the action performed towards it (S-A). Such evidence has been provided using ex-Gaussian distribution analysis to show that different parameters of the reaction time distribution reflect the different processes. Here, using this method, we investigate another difference between these two types of associations: What is the relative durability of these associations across time? Using a task-switching paradigm and by manipulating the lag between the point of the creation of the associations and the test phase, we show that S-A associations have stronger effects on behaviour when the lag between the two repetitions of a stimulus is short. However, classification learning affects behaviour not only in short-term lags but also (and equally so) when the lag between prime and probe is long and the same stimuli are repeatedly presented within a different classification task, demonstrating a remarkable durability of S-C associations.