Precursor processes of human self-initiated action

A gradual buildup of electrical potential over motor areas precedes self-initiated movements. Recently, such "readiness potentials" (RPs) were attributed to stochastic fluctuations in neural activity. We developed a new experimental paradigm that operationalised self-initiated actions as endogenous 'skip' responses while waiting for target stimuli in a perceptual decision task. We compared these to a block of trials where participants could not choose when to skip, but were instead instructed to skip. Frequency and timing of motor action were therefore balanced across blocks, so that conditions differed only in how the timing of skip decisions was generated. We reasoned that across-trial variability of EEG could carry as much information about the source of skip decisions as the mean RP. EEG variability decreased more markedly prior to self-initiated compared to externally-triggered skip actions. This convergence suggests a consistent preparatory process prior to self-initiated action. A leaky stochastic accumulator model could reproduce this convergence given the additional assumption of a systematic decrease in input noise prior to self-initiated actions. Our results may provide a novel neurophysiological perspective on the topical debate regarding whether self-initiated actions arise from a deterministic neurocognitive process, or from neural stochasticity. We suggest that the key precursor of self-initiated action may manifest as a reduction in neural noise

Precursor Processes of Human Self-Initiated Action

A gradual buildup of electrical potential over motor areas precedes self-initiated movements. Recently, such “readiness potentials” (RPs) were attributed to stochastic fluctuations in neural activity. We developed a new experimental paradigm that operationalized self-initiated actions as endogenous ‘skip’ responses while waiting for target stimuli in a perceptual decision task. We compared these to a block of trials where participants could not choose when to skip, but were instead instructed to skip. Frequency and timing of motor action were therefore balanced across blocks, so that conditions differed only in how the timing of skip decisions was generated. We reasoned that across-trial variability of EEG could carry as much information about the source of skip decisions as the mean RP. EEG variability decreased more markedly prior to self-initiated compared to externally-triggered skip actions. This convergence suggests a consistent preparatory process prior to self-initiated action. A leaky stochastic accumulator model could reproduce this convergence given the additional assumption of a systematic decrease in input noise prior to self-initiated actions. Our results may provide a novel neurophysiological perspective on the topical debate regarding whether self-initiated actions arise from a deterministic neurocognitive process, or from neural stochasticity. We suggest that the key precursor of self-initiated action may manifest as a reduction in neural noise

Volition and Action in the Human Brain: Processes, Pathologies, and Reasons

Humans seem to decide for themselves what to do, and when to do it. This distinctive capacity may emerge from an ability, shared with other animals, to make decisions for action that are related to future goals, or at least free from the constraints of immediate environmental inputs. Studying such volitional acts proves a major challenge for neuroscience. This review highlights key mechanisms in the generation of voluntary, as opposed to stimulus-driven actions, and highlights three issues. The first part focuses on the apparent spontaneity of voluntary action. The second part focuses on one of the most distinctive, but elusive, features of volition, namely, its link to conscious experience, and reviews stimulation and patient studies of the cortical basis of conscious volition down to the single-neuron level. Finally, we consider the goal-directedness of voluntary action, and discuss how internal generation of action can be linked to goals and reasons

Specific Relationship Between the Shape of the Readiness Potential, Subjective Decision Time, and Waiting Time Predicted by an Accumulator Model with Temporally Autocorrelated Input Noise

Self-initiated movements are reliably preceded by a gradual buildup of neuronal activity known as the readiness potential (RP). Recent evidence suggests that the RP may reflect subthreshold stochastic fluctuations in neural activity that can be modeled as a process of accumulation to bound. One element of accumulator models that has been largely overlooked in the literature is the stochastic term, which is traditionally modeled as Gaussian white noise. While there may be practical reasons for this choice, we have long known that noise in neural systems is not white – it is long-term correlated with spectral density of the form 1/f^β (with roughly 1 \u3c β \u3c 3) across a broad range of spatial scales. I explored the behavior of a leaky stochastic accumulator when the noise over which it accumulates is temporally autocorrelated. I also allowed for the possibility that the RP, as measured at the scalp, might reflect the input to the accumulator (i.e., its stochastic noise component) rather than its output. These two premises led to two novel predictions that I empirically confirmed on behavioral and electroencephalography data from human subjects performing a self-initiated movement task. In addition to generating these two predictions, the model also suggested biologically plausible levels of autocorrelation, consistent with the degree of autocorrelation in our empirical data and in prior reports. These results expose new perspectives for accumulator models by suggesting that the spectral properties of the stochastic input should be allowed to vary, consistent with the nature of biological neural noise

Feeling ready: neural bases of prospective motor readiness judgements

The idea that human agents voluntarily control their actions, including their spontaneous movements, strongly implies an anticipatory awareness of action. That is, agents should be aware they are about to act before actually executing a movement. Previous research has identified neural signals that could underpin prospective conscious access to motor preparation, including the readiness potential and the beta-band event-related desynchronization. In this study, we ran two experiments to test whether these two neural precursors of action also tracka subjective feeling of readiness. In Experiment 1, we combined a self-paced action task with an intention-probing design where participants gave binary responses to indicate whether they felt they had been about to move when a probe was presented. In Experiment 2, participants reported their feeling of readiness on a graded scale. We found that the feeling of readiness reliably correlates with the beta-band amplitude, but not with the readiness potential

Latent awareness: Early conscious access to motor preparation processes is linked to the readiness potential

An experience of intention to move accompanies execution of some voluntary actions. The Readiness Potential (RP) is an increasing negativity over motor brain areas prior to voluntary movement. Classical studies suggested that the RP starts before intention is consciously accessed as measured by offline recall-based reports, yet the interpretation of the RP and its temporal relation to awareness of intention remain controversial. We designed a task in which self-paced actions could be interrupted at random times by a visual cue that probed online awareness of intention. Participants were instructed to respond by pressing a key if they felt they were actively preparing a self-paced movement at the time of the cue (awareness report), but to ignore the cue otherwise. We show that an RP-like activity was more strongly present before the cue for probes eliciting awareness reports than otherwise. We further show that recall-based reports of the time of conscious intention are linked to visual attention processes, whereas online reports elicited by a probe are not. Our results suggest that awareness of intention is accessible at relatively early stages of motor preparation and that the RP is specifically associated with this conscious experience

Evidence accumulation under uncertainty - a neural marker of emerging choice and urgency

To interact meaningfully with its environment, an agent must integrate external information with its own internal states. However, information about the environment is often noisy. In this study, we identify a neural correlate that tracks how asymmetries between competing alternatives evolve over the course of a decision. In our task participants had to monitor a stream of discrete visual stimuli over time and decide whether or not to act, on the basis of either strong or ambiguous evidence. We found that the classic P3 event-related potential evoked by sequential evidence items tracked decision-making processes and predicted participants' categorical choices on a single trial level, both when evidence was strong and when it was ambiguous. The P3 amplitudes in response to evidence supporting the eventually selected option increased over trial time as decisions evolved, being maximally different from the P3 amplitudes evoked by competing evidence at the time of decision. Computational modelling showed that both the neural dynamics and behavioural primacy and recency effects can be explained by a combination of (a) competition between mutually inhibiting accumulators for the two categorical choice outcomes, and (b) a context-dependant urgency signal. In conditions where evidence was presented at a low rate, urgency increased faster than in conditions when evidence was very frequent. We also found that the readiness potential, a classic marker of endogenously initiated actions, was observed preceding movements in all conditions - even when those were strongly driven by external evidence

From Freedom From to Freedom To: New Perspectives on Intentional Action

There are few concepts as relevant as that of intentional action in shaping our sense of self and the interaction with the environment. At the same time, few concepts are so elusive. Indeed, both conceptual and neuroscientific accounts of intentional agency have proven to be problematic. On the one hand, most conceptual views struggle in defining how agents can adequately exert control over their actions. On the other hand, neuroscience settles for definitions by exclusion whereby key features of human intentional actions, including goal-directness, remain underspecified. This paper reviews the existing literature and sketches how this gap might be filled. In particular, we defend a gradualist notion of intentional behavior, which revolves around the following key features: autonomy, flexibility in the integration of causal vectors, and control

Why neuroscience does not disprove free will

While the question whether free will exists or not has concerned philosophers for centuries, empirical research on this question is relatively young. About 35 years ago Benjamin Libet designed an experiment that challenged the common intuition of free will, namely that conscious intentions are causally efficacious. Libet demonstrated that conscious intentions are preceded by a specific pattern of brain activation, suggesting that unconscious processes determine our decisions and we are only retrospectively informed about these decisions. Libet-style experiments have ever since dominated the discourse about the existence of free will and have found their way into the public media. Here we review the most important challenges to the common interpretation of Libet-style tasks and argue that the common interpretation is questionable. Brain activity preceding conscious decisions reflects the decision process rather than its outcome. Furthermore, the decision process is configured by conditional intentions that participants form at the beginning of the experiment. We conclude that Libet-style tasks do not provide a serious challenge to our intuition of free will

Relation Between Self-reported Reality-monitoring Error Experience and Temporal Fluctuation of Resting-state EEG

Reality monitoring (RM) is the process of making attributional judgments about the source of a memory, in particular, to determine whether a memory is derived from internally generated or externally perceived information. This study examined the relation between self-reported RM in everyday life and temporal fluctuation of the resting-state EEG. A total of 169 undergraduates and graduates took part in the experiment, of whom data of 135 participants were analyzed. First, resting-state spontaneous EEG was recorded for five minutes in the eye-closed resting condition, and then the participants were asked to answer the 32-item Reality-Monitoring Error Experience Questionnaire (RMEEQ) in order to assess the degree to which they experience RM errors in everyday life. The results showed that the coefficient of variation of the beta peak frequency of the spontaneous oscillation at frontal area was larger for those who were more likely to report that they experience RM errors in daily life. On the other hand, the long-range temporal correlation (LRTC) of spontaneous EEG was not correlated with the RMEEQ score. Therefore, it is suggested that the unstable temporal variability of frontal beta oscillation in the resting-state EEG relates to RM measured by RMEEQ.本研究は，国立研究開発法人科学技術振興機構(JST) のCOIプログラムJPMJCE1311，およびJSPS科研費JP19J11638の支援を受けたものです