Elsevier

Neuroscience & Biobehavioral Reviews

Volume 68, September 2016, Pages 639-650
Neuroscience & Biobehavioral Reviews

‘Catching the waves’ – slow cortical potentials as moderator of voluntary action

https://doi.org/10.1016/j.neubiorev.2016.06.023Get rights and content

Highlights

  • The readiness potential (RP) is an ongoing negativity preceding voluntary action.

  • So far the RP was interpreted as a preparatory signal for a self-initiated movement.

  • New evidence can explain the RP also as consequence of prior slow cortical potentials (SCP).

  • This evidence challenges the classical interpretation of experiments on free will.

  • This new hypothesis is in agreement with prior research on SCPs and voluntary action.

Abstract

The readiness potential is an ongoing negativity in the EEG preceding a self-initiated movement by approximately 1.5 s. So far it has predominantly been interpreted as a preparatory signal with a causal link to the upcoming movement. Here a different hypothesis is suggested which we call the selective slow cortical potential sampling hypothesis. In this review of recent research results we argue that the initiation of a voluntary action is more likely during negative fluctuations of the slow cortical potential and that the sampling and averaging of many trials leads to the observed negativity. That is, empirical evidence indicates that the early readiness potential is not a neural correlate of preconscious motor preparation and thus a determinant of action. Our hypothesis thereafter challenges the classic interpretation of the Libet experiment which is often taken as proof that there is no free will. We furthermore suggest that slow cortical potentials are related to an urge to act but are not a neural indicator of the decision process of action initiation.

Introduction

What happens in the brain just before we act is a basic question not only for understanding motor preparation processes but also a key question within the philosophical discussion about free will. The psychophysiological approach to this question is the measurement of electric brain signals prior to action. An example of such a brain signal is the readiness potential (RP), which is derived by the measurement of slow cortical potentials (SCPs) from electrodes on the scalp. SCPs are the slow changing electric brain potentials with frequencies below approximately 1 Hz. The readiness potential is one of the oldest and well-known event-related potentials that can be found in the interval preceding voluntary movement. It was discovered by Kornhuber & Deecke in 1964 (Deecke, 2014, Deecke et al., 1976, Deecke and Kornhuber, 1978, Kornhuber and Deecke, 1965). They asked participants to perform a spontaneous voluntary movement at a self-chosen point in time by simply flexing a finger. They continuously recorded the EEG signals over the course of many movements and then averaged these signals by time-locking them to the onset of action. In the resulting graph one can see an ongoing negativity starting around 1.5 s prior to the self-initiated movement. In control experiments where the finger was flexed passively no such signal was present. This negative potential shift was termed Bereitschaftspotential or readiness potential (RP) and interpreted as the neural signal related to the preparation of the upcoming movement. Preparation is here understood as taking the necessary means in order to be ready for action and this entails several mental conscious and unconscious processes such as decision making, planning and mobilization of resources relating to motor execution.

In the present article, we will review the interpretations of the readiness potential in the light of new empirical data. Evidence conflicting with the classical preparatory interpretation will be presented and contrasted with a more recent interpretation that sees the RP as a neural marker of the decision process to start a movement (Schurger et al., 2012). We will then describe in detail our interpretation of the early part of the RP as having neither a preparatory nor a decision related origin and will provide empirical evidence for this idea. Our hypothesis, called the SCP sampling hypothesis, proposes that (i) self-initiated voluntary action is either facilitated or impeded by the continuous fluctuations of ongoing slow cortical potentials, (ii) that consequently spontaneous voluntary movements are started more likely during a negative increase or negative peak of SCP fluctuations, and (iii) that the averaging of many trials can explain the characteristic curve of the early RP. We will provide empirical evidence for the SCP sampling hypothesis by reviewing our own recent research and we will furthermore complement the picture by a first person perspective based on a neurophenomenological approach. Our interpretation offers a straightforward solution to the question of free will raised by the Libet-experiment. Thereafter, the early RP can no longer be seen as a preparatory signal. The RP is rather an expression of ongoing changes of the readiness to act and thus the classical term ‘readiness’ potential actually captures the essence of this signal.

Section snippets

The readiness potential: classic interpretations and moderating factors

Fifty years ago, Kornhuber and Deecke termed the electrical signal preceding a self-initiated movement ‘readiness potential’ (RP). Their notion of ‘readiness’ has hardly any implications concerning the underlying cognitive and physiological processes. However, the RP was mainly interpreted functionally and goal directed with respect to the upcoming movement, i.e. as an indicator of preparatory processes (Jahanshahi and Hallett, 2003). We will henceforth call this interpretation of the RP the

The Libet experiment

One of the most interesting experimental applications of the RP is its role in the so called Libet experiment. In 1983 Libet replicated the experiment by Kornhuber and Deecke by asking participants to flex a finger at a self-chosen moment while the EEG was recorded (Libet et al., 1983a). In addition, the participants were asked to observe the screen of an oscilloscope on which a spot moved in a circle with a speed of approx. 2.5 s per rotation, simulating a fast-moving clock hand. The

Does the readiness potential reflect movement preparation?

The classical interpretation that the RP is functional with respect to the upcoming movement entails two assumptions. One is that the RP is goal-directed with respect to movement preparation. The second one is that the presence of the RP leads to movement and thus is a neural sign of the decision process. In this section we will review empirical evidence that contradicts the two assumptions.

Regarding the first assumption that the RP reflects movement preparation, there is a variety of studies

Does the readiness potential reflect decision processes?

In 2012 Schurger et al. (2012) proposed a stochastic decision model, which assumes that the RP reflects the decision process to initiate a movement. The authors assumed that the decision is triggered by ongoing stochastic fluctuations in neural activity. If these fluctuations sum up to a certain threshold the decision will take place. Such bounded-integration models are typically applied to perceptual decisions and the authors argue that the same logic might apply for decisions in absence of

The SCP sampling hypothesis

The interpretation that the RP is a neural marker of the decision process has many advantages over the classic interpretation that the RP is related to movement preparation. It is in much better accordance with the set of empirical studies that provide conflicting evidence regarding the interpretation of the RP. However, we will suggest a third interpretation of the RP which we call the Selective Action-Related Slow Cortical Potential Sampling Hypothesis or just SCP Sampling Hypothesis. This

Slow cortical potentials revisited

It is important to note here that the long-time neglected SCPs have more recently gained also interest in context of the search for the neural correlates of consciousness. There are several contributions pointing to correlations between the fMRI BOLD signal and the SCPs (Fox and Raichle, 2007, He et al., 2010, Schroeder and Lakatos, 2009). He et al., (2008) demonstrated correlations between the fMRI BOLD signal and the SCP and argued that the SCP, due to its properties (long-range

From intention to action

The fact that one can obviously intentionally influence the direction of the SCP allows for some interesting speculations regarding the self-regulation of reactivity, sensitivity and volition. On the one hand we have the hypothesis that a shift of the SCP into a negative potential is related to an inner urge or impulse to start an action. On the other hand, we have seen that humans can, at least partially, intentionally modulate their SCP. Combining these two issues brings forward the

Localization of the readiness potential

Our SCP sampling hypothesis stating that the early RP is mainly due to neural fluctuations is in contradiction to the standard interpretation that the RP is a signal of movement preparation. Many studies have investigated the neural dynamics underlying the RP generation and the interesting question will be whether our new interpretation is in accordance with or in contradiction to these findings. In order to do so we will focus mainly on the early part of the RP. This is because the early and

Conclusion and summary: the re-interpretation of the Libet experiment

The readiness potential (RP) has so far been interpreted as an indicator for the preparation of voluntary movements, with preparation defined as necessary neural processing steps that are required before the execution of action can take place. This interpretation is crucial for the ongoing debate on free will around Libet’s famous experiment. Dozens of replications of the Libet experiment have shown that the RP starts approximately 1.5–2.0 s before an intention to act is actually experienced.

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      This seems absurd. Such early RPs, however, do make sense if they are “artifacts” (Jo et al., 2013) of averaging random “stochastic noise” (Schurger et al., 2012) or “slow cortical potentials” (Schmidt et al., 2016) that are always present (no matter what the interval between movements or when the average starts) and that have no necessary relation to movement at all (Alexander et al., 2016)—or anything else for that matter. Maoz et al. (2019) published a study in which they recorded RPs before response choice movements (left or right hand) in the same subjects when they made either arbitrary, meaningless choices (similar to the original Libet paradigm, see Section 2.1.3) or deliberate, meaningful choices.

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