Exploring the internal forward model: action-effect prediction and attention in sensorimotor processing.

Action-effect predictions are believed to facilitate movement based on its association with sensory objectives and suppress the neurophysiological response to self- versus externally generated stimuli (i.e. sensory attenuation). However, research is needed to explore theorized differences in the use of action-effect prediction based on whether movement is uncued (i.e. volitional) or in response to external cues (i.e. stimulus-driven). While much of the sensory attenuation literature has examined effects involving the auditory N1, evidence is also conflicted regarding this component's sensitivity to action-effect prediction. In this study (n = 64), we explored the influence of action-effect contingency on event-related potentials associated with visually cued and uncued movement, as well as resultant stimuli. Our findings replicate recent evidence demonstrating reduced N1 amplitude for tones produced by stimulus-driven movement. Despite influencing motor preparation, action-effect contingency was not found to affect N1 amplitudes. Instead, we explore electrophysiological markers suggesting that attentional mechanisms may suppress the neurophysiological response to sound produced by stimulus-driven movement. Our findings demonstrate lateralized parieto-occipital activity that coincides with the auditory N1, corresponds to a reduction in its amplitude, and is topographically consistent with documented effects of attentional suppression. These results provide new insights into sensorimotor coordination and potential mechanisms underlying sensory attenuation.

The Role of Action-Effect Contingency on Sensory Attenuation in the Absence of Movement.

Stimuli that have been generated by a person's own willed motor actions generally elicit a suppressed electrophysiological, as well as phenomenological, response compared with identical stimuli that have been externally generated. This well-studied phenomenon, known as sensory attenuation, has mostly been studied by comparing ERPs evoked by self-initiated and externally generated sounds. However, most studies have assumed a uniform action-effect contingency, in which a motor action leads to a resulting sensation 100% of the time. In this study, we investigated the effect of manipulating the probability of action-effect contingencies on the sensory attenuation effect. In Experiment 1, participants watched a moving, marked tickertape while EEG was recorded. In the full-contingency (FC) condition, participants chose whether to press a button by a certain mark on the tickertape. If a button press had not occurred by the mark, a sound would be played a second later 100% of the time. If the button was pressed before the mark, the sound was not played. In the no-contingency (NC) condition, participants observed the same tickertape; in contrast, however, if participants did not press the button by the mark, a sound would occur only 50% of the time (NC-inaction). Furthermore, in the NC condition, if a participant pressed the button before the mark, a sound would also play 50% of the time (NC-action). In Experiment 2, the design was identical, except that a willed action (as opposed to a willed inaction) triggered the sound in the FC condition. The results were consistent across the two experiments: Although there were no differences in N1 amplitude between conditions, the amplitude of the Tb and P2 components were smaller in the FC condition compared with the NC-inaction condition, and the amplitude of the P2 component was also smaller in the FC condition compared with the NC-action condition. The results suggest that the effect of contingency on electrophysiological indices of sensory attenuation may be indexed primarily by the Tb and P2 components, rather than the N1 component which is most commonly studied.

Sensory attenuation is modulated by the contrasting effects of predictability and control.

Self-generated stimuli have been found to elicit a reduced sensory response compared with externally-generated stimuli. However, much of the literature has not adequately controlled for differences in the temporal predictability and temporal control of stimuli. In two experiments, we compared the N1 (and P2) components of the auditory-evoked potential to self- and externally-generated tones that differed with respect to these two factors. In Experiment 1 (n = 42), we found that increasing temporal predictability reduced N1 amplitude in a manner that may often account for the observed reduction in sensory response to self-generated sounds. We also observed that reducing temporal control over the tones resulted in a reduction in N1 amplitude. The contrasting effects of temporal predictability and temporal control on N1 amplitude meant that sensory attenuation prevailed when controlling for each. Experiment 2 (n = 38) explored the potential effect of selective attention on the results of Experiment 1 by modifying task requirements such that similar levels of attention were allocated to the visual stimuli across conditions. The results of Experiment 2 replicated those of Experiment 1, and suggested that the observed effects of temporal control and sensory attenuation were not driven by differences in attention. Given that self- and externally-generated sensations commonly differ with respect to both temporal predictability and temporal control, findings of the present study may necessitate a re-evaluation of the experimental paradigms used to study sensory attenuation.

Individual differences in sensory integration predict differences in time perception and individual levels of schizotypy.

To interact functionally with our environment, our perception must locate events in time, including discerning whether sensory events are simultaneous. The Temporal Binding Window (TBW; the time window within which two stimuli tend to be integrated into one event) has been shown to relate to individual differences in perception, including schizotypy, but the relationship with subjective estimates of duration is unclear. We compare individual TBWs with individual differences in the filled duration illusion, exploiting differences in perception between empty and filled durations (the latter typically being perceived as longer). Schizotypy has been related to both these measures and is included to explore a potential link between these tasks and enduring perceptual differences. Results suggest that individuals with a narrower TBW make longer estimates for empty durations and demonstrate less variability in both conditions. Exploratory analysis of schizotypy data suggests a relationship with the TBW but is inconclusive regarding time perception.

How much does emotional valence of action outcomes affect temporal binding?

Temporal binding refers to the compression of the perceived time interval between voluntary actions and their sensory consequences. Research suggests that the emotional content of an action outcome can modulate the effects of temporal binding. We attempted to conceptually replicate these findings using a time interval estimation task and different emotionally-valenced action outcomes (Experiments 1 and 2) than used in previous research. Contrary to previous findings, we found no evidence that temporal binding was affected by the emotional valence of action outcomes. After validating our stimuli for equivalence of perceived emotional valence and arousal (Experiment 3), in Experiment 4 we directly replicated Yoshie and Haggard's (2013) original experiment using sound vocalizations as action outcomes and failed to detect a significant effect of emotion on temporal binding. These studies suggest that the emotional valence of action outcomes exerts little influence on temporal binding. The potential implications of these findings are discussed.

EEG indices of reward motivation and target detectability in a rapid visual detection task.

A large corpus of data has demonstrated the sensitivity of behavioral and neural measures to variation in the availability of reward. The present study aimed to extend this work by exploring reward motivation in an RSVP task using complex satellite imagery. We found that reward motivation significantly influenced neural activity both in the preparatory period and in response to target images. Pre-stimulus alpha activity and, to a lesser degree, P3 and CNV amplitude were found to be significantly predictive of reward condition on single trials. Target-locked P3 amplitude was modulated both by reward condition and by variation in target detectability inherent to our task. We further quantified this exogenous influence, showing that P3 differences reflected single-trial variation in P3 amplitude for different targets. These findings provide theoretical insight into the neural indices of reward in an RSVP task, and have important applications in the field of satellite imagery analysis.

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.

Perceptual training modifies temporal sensitivity and a sense of agency.

Perceptual training has been argued to be a potential means to modify temporal sensitivity (the ability to detect a time-based discrepancy between two stimuli) with previous studies providing preliminary evidence that perceptual training can lead to increased temporal sensitivity. However, previous studies have not employed a control group and therefore cannot rule out the possibility that the observed effects are due to repeated completion of the task, rather than the training itself. Moreover, despite temporal sensitivity being suggested to be an important aspect of the sense of agency, the effects of perceptual training on the sense of agency have not been explored. Therefore, this study aimed to explore the effects of perceptual training on the sense of agency and replicate previously observed effects on temporal sensitivity while utilizing a more rigorous methodology. Given the existing literature, it was predicted that the sense of agency and temporal sensitivity will be enhanced following perceptual training. Temporal sensitivity was only weakly modified by perceptual training when compared to the control condition. Sense of agency was significantly modulated by perceptual training, over and above the control condition. This study's findings present novel evidence indicating that perceptual training can influence high-level processes such as the sense of agency and temporal sensitivity.

One action system or two? Evidence for common central preparatory mechanisms in voluntary and stimulus-driven actions.

Human behavior is comprised of an interaction between intentionally driven actions and reactions to changes in the environment. Existing data are equivocal concerning the question of whether these two action systems are independent, involve different brain regions, or overlap. To address this question we investigated whether the degree to which the voluntary action system is activated at the time of stimulus onset predicts reaction times to external stimuli. We recorded event-related potentials while participants prepared and executed left- or right-hand voluntary actions, which were occasionally interrupted by a stimulus requiring either a left- or right-hand response. In trials where participants successfully performed the stimulus-driven response, increased voluntary motor preparation was associated with faster responses on congruent trials (where participants were preparing a voluntary action with the same hand that was then required by the target stimulus), and slower responses on incongruent trials. This suggests that early hand-specific activity in medial frontal cortex for voluntary action trials can be used by the stimulus-driven system to speed responding. This finding questions the clear distinction between voluntary and stimulus-driven action systems.

Correction: The effect of cognitive effort on the sense of agency.

[This corrects the article DOI: 10.1371/journal.pone.0236809.].

ERP correlates of action effect prediction and visual sensory attenuation in voluntary action.

Sensory attenuation of voluntary action effects has been widely reported in both somatosensory and auditory domains. However, relatively little research has focused on physiological measures of sensory attenuation of visual action effects. One previous study found, perhaps surprisingly, that both auditory and visual sensory attenuation were manifested as decreased ERP amplitude over the vertex. The present study aimed to extend these findings using a novel paradigm in which voluntary actions were either associated with a visual action effect or to no effect. Crucially, this allowed us to explore both sensory attenuation (by comparing ERPs to action-triggered versus externally triggered stimuli) and action effect prediction (by comparing actions that triggered a stimulus with actions that did not). With regard to sensory attenuation, we found that attenuation of cortical responses to visual action effects was manifested in a reduced activation of a frontoparietal network, from 150 ms after stimulus. Differences between actions that produced an effect and those that did not were observed in lateralized motor potentials and may reflect the cortical correlates of the action effect prediction. We also observed a re-activation of lateralized motor activity following onset of the action effect, suggesting a common representation of action effects in visual and motor cortices. Taken together, these findings help to elucidate the cortical mechanisms of voluntary action as well as their sensory consequences and inform how our interaction with the external world is processed and controlled.

Individual differences in alpha frequency are associated with the time window of multisensory integration, but not time perception.

Previous research provides some preliminary evidence to link the temporal binding window, the time frame within which multisensory information from different sensory modalities is integrated, and time perception. In addition, alpha peak frequency has been proposed to be the neural mechanism for both processes. However, these links are not well established. Hence, the aim of the current study was to explore to what degree, if any, time perception, the temporal binding window and the alpha peak frequency are related. It was predicted that as the width of the temporal binding window increases the size of the filled duration illusion increases and the alpha peak frequency decreases. We observed a significant relationship between the temporal binding window and peak alpha frequency. However, time perception was not linked with either of these. These findings are discussed with respect to the possible underlying mechanisms of multisensory integration and time perception.

Sensory attenuation in the absence of movement: Differentiating motor action from sense of agency.

Sensory attenuation is the phenomenon that stimuli generated by willed motor actions elicit a smaller neurophysiological response than those generated by external sources. It has mostly been investigated in the auditory domain, by comparing ERPs evoked by self-initiated (active condition) and externally-generated (passive condition) sounds. The mechanistic basis of sensory attenuation has been argued to involve a duplicate of the motor command being used to predict sensory consequences of self-generated movements. An alternative possibility is that the effect is driven by between-condition differences in participants' sense of agency over the sound. In this paper, we disambiguated the effects of motor-action and sense of agency on sensory attenuation with a novel experimental paradigm. In Experiment 1, participants watched a moving, marked tickertape while EEG was recorded. In the active condition, participants chose whether to press a button by a certain mark on the tickertape. If a button-press had not occurred by the mark, then a tone would be played 1 s later. If the button was pressed prior to the mark, the tone was not played. In the passive condition, participants passively watched the animation, and were informed about whether a tone would be played on each trial. The design for Experiment 2 was identical, except that the contingencies were reversed (i.e., a button-press by the mark led to a tone). The results were consistent across the two experiments: while there were no differences in N1 amplitude between the active and passive conditions, the amplitude of the Tb component was suppressed in the active condition. The amplitude of the P2 component was enhanced in the active condition in both Experiments 1 and 2. These results suggest that motor-actions and sense of agency have differential effects on sensory attenuation to sounds and are indexed with different ERP components.

Temporal binding window and sense of agency are related processes modifiable via occipital tACS.

The temporal binding window refers to the time frame within which temporal grouping of sensory information takes place. Sense of agency is the feeling of being in control of one's actions, and their associated outcomes. While previous research has shown that temporal cues and multisensory integration play a role in sense of agency, no studies have directly assessed whether individual differences in the temporal binding window and sense of agency are associated. In all three experiments, to assess sense of agency, participants pressed a button triggering, after a varying delay, the appearance of the circle, and reported their sense of agency over the effect. To assess the temporal binding window a simultaneity judgment task (Experiment 1) and a double-flash illusion task (Experiment 2 and 3) was also performed. As expected, the temporal binding window correlated with the sense of agency window. In Experiment 3, these processes were modulated by applying occipital tACS at either 14Hz or 8Hz. We found 14Hz tACS stimulation was associated with narrower temporal biding window and sense of agency window. Our results suggest the temporal binding window and the time window of sense of agency are related. They also point towards a possible underlying neural mechanism (alpha peak frequency) for this association.

The relation between consciousness and attention: an empirical study using the priming paradigm.

Dehaene, Changeux, Naccache, Sackur, and Sergent (2006) and Koch and Tsuchiya (2007) recently proposed taxonomies that distinguish between four processing states, based on bottom-up stimulus strength and top-down attentional amplification. The aim of the present study was to empirically test these processing states using the priming paradigm. Our results showed that attention (prime attended or not) and stimulus strength (prime presented subliminally or not) significantly modulated priming effects: either receiving top-down attention or possessing sufficient bottom-up strength was a prerequisite for a stimulus to elicit priming. When both top-down attention and sufficient bottom-up strength were present, the priming effect was boosted. The origins of the observed priming effects also varied between different processing states. We can conclude that our empirical study using the priming paradigm confirmed the presence of four processing states, which displayed a differential pattern of response priming effects and differential origins of the response priming effects.

Behavioral and neural dynamics of cognitive control in the context of rumination.

Rumination is a characteristic feature of several clinical disorders (e.g., major depressive disorder, insomnia disorder). Emerging evidence suggests that a reduced flexibility in the balance between proactive and reactive control might be related to trait rumination. This study aimed to investigate the proactive-reactive control balance in the context of trait rumination. In the current study, we investigated behavioral performance and event-related potentials (ERPs) while participants were performing an AX- Continuous Performance Task, to evaluate whether a shift towards more reactive control (i.e., conflict monitoring and resolution) at the expense of proactive control (i.e., maintenance and updating of task-relevant information) is associated with increased trait rumination. Our behavioral results as well as our ERP results did not demonstrate that a shift towards more reactive control at the expense of proactive control was associated with increased trait rumination. Future research is needed to investigate the proactive-reactive control balance in the context of trait rumination. This study is the first to explore the recruitment dynamics of cognitive control using behavioral as well as electrophysiological measures in the context of rumination.

Learning to fear pain after observing another's pain: An experimental study in schoolchildren.

BACKGROUND: Children of individuals with chronic pain have an increased vulnerability to experience pain problems, possibly through observation of pain in their parents. As pain-related fear (PRF) is a critical factor in the development and maintenance of chronic pain, the current experimental study examined the acquisition of PRF through observational learning and subsequent extinction after first-hand experience of the feared stimulus. METHODS: Healthy children (8-16 years) observed either their mother or a stranger performing two cold pressor tasks (CPT) filled with coloured water. In a differential conditioning procedure, one colour (CS+) was combined with genuine painful facial expressions and the other colour (CS-) with neutral facial expressions. Following this observation phase, children performed both CPTs (10°C) themselves. RESULTS: Children expected the CS+ to be more painful than the CS- and they reported being more afraid and hesitant to immerse in the CS+ compared to the CS-. Moreover, this fear was reflected in children's level of arousal in anticipation of CPT performance. This learned association extinguished after performing both CPTs. Effects were not moderated by whether the child observed their mother or a stranger, by the child's pain catastrophizing, trait PRF or trait anxiety. Remarkably, learning effects increased when the child perceived a larger difference between the model's painful and neutral facial expressions. CONCLUSIONS: This study provides evidence for observational learning of PRF and subsequent extinction in schoolchildren. This acquisition of PRF by observing parental pain may contribute to vulnerabilities in children of parents with chronic pain. SIGNIFICANCE: Children may acquire pain-related fear by observing pain in others and this learned fear can diminish after first-hand experience. Remarkably, observational learning did not depend on the children's relationship with the model, but it did depend on the intensity of pain that is perceived. A better understanding of the impact of observing (parental) pain may help clarify the intergenerational transmission of risk for pain and inform the development of preventive programs.

The effect of cognitive effort on the sense of agency.

While we are performing a demanding cognitive task, not only do we have a sense of cognitive effort, we are also subjectively aware that we are initiating, executing and controlling our thoughts and actions (i.e., sense of agency). Previous studies have shown that cognitive effort can be both detrimental and facilitative for the experienced sense of agency. We hypothesized that the reason for these contradictory findings might lie in the use of differential time windows in which cognitive effort operates. The current study therefore examined the effect of cognitive effort exerted on the current trial, on the previous trial or across a block of trials on sense of agency, using implicit (Experiment 1) and explicit (Experiment 2) measures of sense of agency. We showed that the exertion of more cognitive control on current trials led to a higher explicit sense of agency. This surprising result was contrasted to previous studies to establish potential reasons for this surprising finding and to formulate recommendations for future studies.

Prefrontal transcranial alternating current stimulation improves motor sequence reproduction.

Cortical activity in frontal, parietal, and motor regions during sequence observation correlates with performance on sequence reproduction. Increased cortical activity observed during observation has therefore been suggested to represent increased learning. Causal relationships have been demonstrated between M1 and motor sequence reproduction and between parietal cortex and bimanual learning. However, similar effects have not been reported for frontal regions despite a number of reports implicating its involvement in encoding of motor sequences. Investigating causal relations between cortical activity and reproduction of motor sequences in parietal, frontal and primary motor regions can disentangle whether specific regions during simple observation can be selectively ascribed to encoding or reproduction or both. We designed a sensorimotor paradigm that included a strong motor sequence component, and tested the impact of individually adjusted transcranial alternating current stimulation (IAF-tACS) to prefrontal, parietal, and primary motor regions on electroencephalographic motor rhythms (alpha and beta bandwidths) during motor sequence observation and the ability to reproduce the observed sequences. Independently of the stimulated region, IAF-tACS led to a reduction in suppression in the lower beta-range relative to sham. Prefrontal IAF-tACS however, led to significant improvement in motor sequence reproduction, pinpointing the crucial role of prefrontal regions in motor sequence reproduction.