Gethin Hughes

Mechanisms of intentional binding and sensory attenuation: The role of temporal prediction, temporal control, identity prediction, and motor prediction.

Sensory processing of action effects has been shown to differ from that of externally triggered stimuli, with respect both to the perceived timing of their occurrence (intentional binding) and to their intensity (sensory attenuation). These phenomena are normally attributed to forward action models, such that when action prediction is consistent with changes in our environment, our experience of these effects is altered. Although much progress has been made in recent years in understanding sensory attenuation and intentional binding, a number of important questions regarding the precise nature of the predictive mechanisms involved remain unanswered. Moreover, these mechanisms are often not discussed in empirical papers, and a comprehensive review of these issues is yet to appear. This review attempts to fill this void. We systematically investigated the role of temporal prediction, temporal control, identity prediction, and motor prediction in previous published reports of sensory attenuation and intentional binding. By isolating the individual processes that have previously been contrasted and incorporating these experiments with research in the related fields of temporal attention and stimulus expectation, we assessed the degree to which existing data provide evidence for the role of forward action models in these phenomena. We further propose a number of avenues for future research, which may help to better determine the role of motor prediction in processing of voluntary action effects, as well as to improve understanding of how these phenomena might fit within a general predictive processing framework. Furthermore, our analysis has important implications for understanding disorders of agency in schizophrenia.

Action effect anticipation: Neurophysiological basis and functional consequences

Voluntary actions are thought to be selected with respect to their intended goal. Converging data suggests that medial frontal cortex plays a crucial role in linking actions to their predicted effects. Recent neuroimaging data also suggests that during action selection, the brain pre-activities the representation of the predicted action effect. We review evidence of action effect prediction, both in terms of its neurophysiological basis as well as its functional consequences. By assuming that action preparation includes activation of the predicted sensory consequences of the action, we provide a mechanism to understand sensory attenuation and intentional binding. In this account, sensory attenuation results from more difficult discrimination between the observed action effect and the pre-activation of the predicted effect, as compared to when no (or incorrect) prediction is present. Similarly, a predicted action effect should also reach the threshold of awareness faster (intentional binding), if its perceptual representation is pre-activated. By comparing this potential mechanism to mental imagery and repetition suppression we propose a possible neural basis for the processing of predicted action effects.

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.

Intentional binding is driven by the mere presence of an action and not by motor prediction.

Intentional binding refers to the fact that when a voluntary action produces a sensory outcome, action and outcome are perceived as being closer together in time. This phenomenon is often attributed, at least partially, to predictive motor mechanisms. However, previous studies failed to unequivocally attribute intentional binding to these mechanisms, since the contrasts that have been used to demonstrate intentional binding covered not only one but two processes: temporal control and motor identity prediction. In the present study we aimed to isolate the respective role of each of these processes in the emergence of intentional binding of action-effects. The results show that motor identity prediction does not modulate intentional binding of action-effects. Our findings cast doubts on the assumption that intentional binding of action effects is linked to internal forward predictive process.

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.

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.

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.

Action prediction modulates both neurophysiological and psychophysical indices of sensory attenuation

Sensory attenuation refers to the observation that stimuli that are predicted based on one’s action are attenuated. This phenomenon has primarily been observed as a neurophysiological phenomenon, with reduced Event-Related Potential (ERP) (e.g., Bäss et al., 2008) and BOLD (e.g., Blakemore et al., 1998). However, psychophysical investigations (e.g., Sato, 2008; Cardoso-Leite et al., 2010; Roussel et al., 2013) have confirmed that action prediction also influences the perception of sensory action effects. The present study recorded both neurophysiological and psychophysical measures in a single experiment, to confirm whether the two phenomena are related. In addition, by measuring the ERP modulations of both stimulus contrast and prediction congruency, we sought to directly relate the neurophysiological phenomenon to the magnitude of sensory processing in the brain. Participants performed left- and right-hand voluntary actions that were previously associated with the letters A and H. In the test phase, participants were presented with these same two letters, at one of two possible contrasts. Participants were required to report which of the two possible contrasts had been presented. We observed both reduced contrast discrimination (in line with Roussel et al., 2013) and a reduced ERP response for congruent action-effects. Furthermore, our congruency modulation was observed on the same component that differed as a function of stimulus contrast. Taken together these results strongly suggest that neurophysiological indices of sensory attenuation reflect reduced sensory processing of voluntary action effects.

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.

Disentangling conscious and unconscious processing: a subjective trial-based assessment approach

The most common method for assessing similarities and differences between conscious and unconscious processing is to compare the effects of unconscious (perceptually weak) stimuli, with conscious (perceptually strong) stimuli. Awareness of these stimuli is then assessed by objective performance on prime identification tasks. While this approach has proven extremely fruitful in furthering our understanding of unconscious cognition, it also suffers from some critical problems. We present an alternative methodology for comparing conscious and unconscious cognition. We used a priming version of a Stroop paradigm and after each trial, participants gave a subjective rating of the degree to which they were aware of the prime. Based on this trial-by-trial awareness assessment, conscious, uncertain, and unconscious trials were separated. Crucially, in all these conditions, the primes have identical perceptual strength. Significant priming was observed for all conditions, but the effects for conscious trials were significantly stronger, and no difference was observed between uncertain and unconscious trials. Thus, awareness of the prime has a large impact on congruency effects, even when signal strength is controlled for.