experiment von libet et al. (1983)

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The libet experiment and its implications for conscious will.

Dr Peter Clarke considers whether the experiments of Benjamin Libet call into question the reality of human will. Although quite a technical paper, Dr Clarke makes it clear that there is far more to the discussion, and far more uncertainty, than is allowed in the popular interpretations of these experiments. Whether or not you hold the same philosophical position on monism and dualism as Dr Clarke, this paper will help you challenge interpretations of Libet's experiments that deny the reality of human conscious will.

Summary: A famous experiment of Benjamin Libet and his colleagues has been interpreted as showing that our brains initiate voluntary movements before we are aware of having decided to move, and that this calls into question the efficacy of our wills. These claims have been contested by many neuroscientists and philosophers. This paper provides an introduction to the controversy.

The neurophysiological experiments of Benjamin Libet and his collaborators in the 1980s [1] have been interpreted by the authors and many others as showing that our brains initiate conscious voluntary movements as well as the will to move before we are consciously aware of the will to move. I shall refer to this claim as the Libet claim for brevity. It is controversial, but if valid would have important implications for our understanding of how the mind relates to the brain and for the role of conscious will in the performance of voluntary actions. Before going into details about the Libet experiment, I must first provide some information about the mind-brain relationship and the neurophysiology of voluntary movement.

The Mind-Brain Relationship and the Libet Claim

It is generally accepted that the electrical activity of our brains underlies our conscious thought, including our decision making. How a physical thing, the brain, can be the basis of consciousness is a subject of debate that has given rise to many different philosophical positions, but these can be grouped in two main categories: dualism and monism.

So great was the influence of Descartes on western philosophy that, from the late seventeenth century until around 1950 or so, most westerners accepted some form of interactive dualism, involving an immaterial soul acting on a material brain. Since then this view has lost favour, for a variety of reasons, including the arguments of philosophers such as Ryle, Place and Feigl. In addition, atheistic materialists rejected it because it invokes a nonmaterial entity, but so did most Christian academics, because advances in the analysis of biblical texts in the mid twentieth century and since tended to support a monistic conception of man, not a dualistic one. [2] This realisation was not entirely revolutionary, because there had always been a monistic strand in Christian thought due to the influence of Thomas Aquinas. Thus, during his Gifford Lectures in 1956-57, Anglican theologian Austin Farrer criticised the dualistic views of neurobiologist (and future Nobel prize-winner) John Eccles, writing:

We will have nothing to do with the fantastic suggestion, that what the supersensitive ‘reactors’ in the cortex react to, is the initiative of a virtually disembodied soul. To what, then, are we to say that they do react? What else, than to the motions of the embodied soul, that is to say, other motions in the same nervous system? [3]

For these reasons, with a few exceptions, [4] most modern philosophers and neuroscientists, whether theist or atheist, accept some form of monism, but this does not have to involve eliminative materialism that rejects mind as illusory. Many theists, agnostics and atheists adopt more moderate monist positions such as two aspect monism, according to which our subjective, first-personal, account of our inner life and neuroscience’s objective, third-personal account of our brain’s activity refer to complementary aspects of a single entity. [5] An alternative view is the mind-brain identity theory, according to which the mind and the brain’s activity are considered to be the same entity, not two aspects of the same entity. I prefer two-aspect monism because mind-brain identity seems to me linguistically problematic, but the two formulations make identical predictions at the level of brain function.

if brain events come first, this would support epiphenomenalism, the view that mind events are mere by-products of brain events, with no causal role.

A striking aspect of the Libet claim is that it goes against the main versions of both dualism and monism. Cartesian dualism predicts that mind events should precede brain events, since the nonphysical mind (or soul etc.) is considered to be the real source of our decisions. Two-aspect monism and mind-brain identity theory both predict that mind and brain events should be synchronous, since mind-level descriptions and brain-level descriptions are considered complementary (and equally valid) accounts of the same processes. But if brain events come first, this would support epiphenomenalism, the view that mind events are mere by-products of brain events, with no causal role. This would deny the causal efficacy of conscious will.

The Neurophysiology of Voluntary Movement

It is important to be clear about what is, and is not, being claimed when a movement is called voluntary. Even though these movements involve, by definition, an act of conscious will, that is not to say that every aspect of the movement is conscious or willed. For example, the movements of a tennis player as she serves are voluntary, but their control involves many automatic subroutines in the cerebellum and elsewhere. Furthermore, to claim that conscious acts of will initiate voluntary movements is not to deny that the acts of will arise out of brain processes that are largely unconscious. [6]

What is the nature of the ‘I’ (or self) that willed the movement and performed it? The use of such terms does not imply dualism. The ‘I’ (or self, or mind etc.) is generally conceived as being embodied in (or emerging from) the brain’s activity.

The neural circuits involved in voluntary motor control are exceedingly complicated, and I here give only some simplified information that is necessary for understanding the Libet experiment. Voluntary movements are controlled primarily by the motor cortex (in the back part of the frontal lobe – Fig. 1) but in cooperation with many other motor centres including the basal ganglia and the cerebellum. Motor commands are sent from the primary motor cortex (and to some extent from other areas) to motoneurons in the brainstem and spinal cord, which in turn control the muscles. The initiation and programming of movements depend on activity in many areas including the supplementary motor area (Fig. 1) and the preSMA, and several areas in the parietal cortex. These areas feed directly or indirectly into the premotor cortex and motor cortex. Electrical stimulation of the motor areas produces movements, but not the will to move. In contrast, electrical stimulation of areas BA-39 and BA-40 in the parietal lobe (Fig. 1) elicits the will to move, but does not cause a movement. [7]

The Libet Experiment, a Challenge to the Role of Conscious Will

An important background to the Libet experiment was the discovery in the 1960s that, before people make a voluntary movement, there is a slow build-up of electrical potential measured from the skull over the motor cortex, beginning as much as a second earlier for simple movements and even longer for complex series of movements. [8] This electrical change is called the readiness potential (RP).

Libet was interested in the relative timing of the RP compared with the movement and the conscious decision to move. He therefore asked his experimental subjects to perform simple movements, in most cases flexion of the fingers or wrist, and to estimate the time of conscious awareness of the urge (or will or decision) to move (W) by reporting the position of a spot moving in a circle on an oscilloscope screen. They were told to perform the movement whenever they felt like doing so, and to pay close attention to the time when they were first aware of the ‘urge to move’. He also recorded the RP by electroencephalography, and the time of the movement itself was estimated from the electromyogram [ measurement of the electrical impulses in muscles - ed] . Libet found that time W came only about 200 msec before the movement, whereas the RP began much earlier, usually about 550 msec before the movement (Fig. 2). The fact that the change in brain potential occurred before the conscious decision was interpreted by Libet and by many commentators to imply that our conscious decision to act is not the true cause of the movement. They deduced that conscious will is too slow to make things happen, and that volitional acts must result from unconscious processes in the brain, not from conscious willing. This seemed to imply that our intuitive notion of conscious will must be an illusion.

There appeared to be a small loophole in that Libet’s subjects still had the power to veto a movement in the 200 msec between time W and the movement. He therefore argued that even though the initiation of the movement was not the result of conscious will, its vetoing was. This argument has not attracted great interest, but was supported by eminent free-will philosopher Robert Kane. [9]

The Libet experiment provoked considerable interest and intense controversy, and stimulated further experimentation.

Single Neuron Recordings During the Libet Experiment

The overall conclusion on timing has to be that the problems have not so far been resolved.

It is rarely possible to record from single neurons in the brains of humans, but this can occasionally be done in epilepsy patients using electrodes that have been implanted to localise the zones that cause seizures. Thus, remarkably, Itzhak Fried and his collaborators managed to record from more than 1,000 neurons in the medial frontal cortex of epilepsy patients (and especially in the supplementary motor area, which generates most of the early part of the RP) as they performed the Libet experiment. It was found that a few neurons changed their firing rate (by an increase or a decrease) almost 1.5 sec before time W, and more and more neurons did so over the following 1.5 sec, with about 25% of the neurons firing several tenths of a second before W. The authors conclude that their findings support the view that the experience of will emerges as the culmination of premotor activity starting several hundreds of msec before awareness. [10]

Criticisms of the Libet Claim

Despite the fame of the Libet experiment and its frequent acceptance in popular and semi-popular writings, it has been the subject of intense controversy. Indeed, most specialists in the philosophy of free will who have addressed the Libet claim have rejected it. [11] Most of the criticisms focused on difficulties of judging the time of awareness, of interpreting the RP, or of philosophical interpretation, as is discussed below.

Problems of judging the time of awareness

It was central to Libet’s claim that the readiness potential began distinctly before time W. The published data of several groups do indeed support this claim, but critics have objected to the use of subjective recall after the event, because there is evidence that this can be very unreliable. Furthermore, those such as Alfred Mele [12] who have tried the experiment for themselves have found that W is difficult to define. I have done this too, and you may wish to try it using a ‘clock’ available on the web. [13] When I try this, I find it very hard to judge the precise time when I decided to move my finger / wrist. It would be useful to quantify the reliability of our judgements, but this is difficult for a purely subjective decision. For this reason, several research groups have instead measured the reliability of timing judgements for perceptual events, which is easier to do. Results have been variable, but several groups found serious biases, [14] raising doubts about the interpretation of the Libet experiment. A different critique of the timing was made by Dennett and Kinsbourne, [15] who point out that Libet’s experiment involves an attention shift from the participants’ subjective intention to the clock, which may have introduced temporal mismatches between the felt experience of will and the perceived position of the clock hand.

To try to solve these problems, Matsuhashi and Hallett devised an alternative methodology for estimating time W. They found that the RP (which they called BP1) occurred before W in only about two thirds of the subjects; worse, the lateralised RP (LRP) that we shall discuss below, always occurred after W. [16]

In view of the controversy about the measurement of subjective timing, considerable attention was devoted in the public media to a paper published in Nature Neuroscience that used brain scanning technology (functional magnetic resonance imaging – fMRI) in a Libet-like experimental paradigm, and included in the summary a claim that a "decision can be encoded in brain activity of prefrontal and parietal cortex almost 10 sec before it enters awareness" . [17] After all the subtle debate about a few hundreds of milliseconds, 10 sec was an enormous amount of time, and the wording of the abstract gave the impression that the temporal priority of the neural decision with respect to the subjective one was finally established. I assume that some journalists and bloggers only had access to the abstract (available free on the web) and not to the full paper, because the main text made only the much weaker claim that the activity of prefrontal and parietal cortex was correlated with the decision (to use the left or right hand) with 60% prediction accuracy, up to 10 sec before the conscious decision. That is very different! To reflect a neural decision, the correlation would need to be at 100%, not 60%. The paper provided valuable information about brain activity leading ultimately to a decision, but did nothing to rescue the Libet experiment from the criticisms about timing.

Doubts as to whether the readiness potential reflects a decision to move

The Libet claim assumes that the RP reflects a neural ‘decision’ to move, and that the neural activity underlying the RP causes both the will to move and the movement. Even if such causality could be demonstrated, this would not strictly be sufficient to validate the Libet claim, because the decision must presumably be caused by a chain of preceding neural events, and the RP might reflect some of these. But the Libet claim certainly assumes causality. This is part of the claim, and it has never been proved.

Libet et al. explicitly pointed out that their conclusions applied only to spontaneous, rapidly performed movements

To be precise, we are really talking about the earliest part of the RP, because the timing argument focuses on the RP’s onset. To attribute such a decisional and causal role to this earliest part of the RP seems surprising, because it originates mainly in the SMA (Fig. 1), which has been known for more than thirty years to be strongly activated when subjects ‘programme’ (imagine) a complex movement without actually performing it. [18] This is not to deny that activity in SMA can cause movements in some cases, such as when it is stimulated electrically, but it cannot be assumed that the earliest part of the RP necessarily reflects neural processes underlying a decision to move. And there are at least six specific reasons to doubt this.

First, even though electrical stimulation of the SMA can cause movements, it does not cause a will to move, which requires stimulation of parietal areas. [19] This suggests that the RP does not cause the will to move.

Second, if the RP truly caused the conscious will and the movement, one would expect trial-to-trial variations in the onset of the RP to correlate with trial-to-trial variations in time W; that is to say that trials with an early RP should also have an early W. Haggard and Eimer tested this, using a variant of the Libet experiment, and found there was little correlation, ruling out the RP as a cause of the will or decision to move. They did, however, find that the ‘lateralized readiness potential’ (LRP: i.e. the RP from the cortex on the opposite side relative to the movement minus the RP from the same side) gave a positive correlation, suggesting that the brain processes underlying the LRP might cause the will to move. [20] At the time, their paper did not seem to challenge the Libet claim, because the LRP seemed to fulfil the role formerly attributed to the RP. However, the LRP occurs later than the RP, and subsequent experiments have sometimes found that the LRP occurs even after time W as is discussed above, [21] so the LRP seems a fragile candidate to replace the RP.

Third, Alfred Mele has pointed out a flaw in Libet’s experimental paradigm that vitiates attempts to deduce a causal influence between the RP and the movement (and the will to move). [22] In all Libet’s experiments, the permanent storage of electroencephalographic data was triggered by the finger / wrist movements. This was necessary as part of the averaging procedure that is necessary to detect the RP, which would otherwise be masked by other concurrent activity in the EEG. If there was no movement, the data were not stored, so any RPs that occurred without being followed by movements would not have been detected. If such RPs without movement did occur, then RPs are not sufficient to cause movements, and more probably reflected brain activity occurring prior to the decision to move. This possibility is difficult to evaluate, because the averaging procedure has to be triggered at a moment defined by the movement.

Fourth, experiments by Hermann et al. cast further doubt on the interpretation of the RP as causally related to the decision and movement. [23] These researchers used a modified version of the Libet experimental paradigm, in which the participants were instructed to press one of two buttons, depending on a presented stimulus. An RP occurred well before the motor response, as in the Libet experiment. But, importantly, it occurred even before the stimulus presentation, so it clearly did not reflect a decision as to which button to press. The authors argue that the RP does not specifically determine the movement, but may reflect a general expectation (which is indeed what the RP was initially thought by Kornhuber and Deecke to reflect, not a decision but a state of readiness, hence its name).

Fifth, Trevena and Miller devised a modified version of the Libet experiment in which participants made spontaneous decisions to move, or not, and found that the RP was no stronger before a decision to move than before a decision not to move, which is not what one would expect if the RP reflected a neural decision to move. [24]

Sixth, computational analysis suggests that the neural decision to move occurs only very late during the time-course of the RP, not at its onset. [25]

Debate about the philosophical interpretation

Even if the Libet claim is accepted – which is very controversial, as we have seen – there is also debate about the philosophical interpretation.

Libet ... maintained that conscious will can still play a genuine role in the vetoing of initiated acts.

I have here used systematically the term ‘conscious will’ rather than ‘free will’ to avoid the broader philosophical associations of the latter term. Nevertheless, many supporters of the Libet claim, including Libet himself [26] , have used the term ‘free will’. This has aroused further controversy, because many critics have argued that Libet’s experimental paradigm was irrelevant to the question of free will. When we talk about free will, we are usually referring to choices among a variety of options, often with moral implications, and this may require careful deliberation over a period of minutes or hours or days. The Libet experiment is just the opposite. The subject was not making a moral decision, and was not even deciding whether to move, but only when. Moreover, the subjects were specifically instructed not to deliberate but to act spontaneously, and in their original 1983 paper Libet et al. explicitly pointed out that their conclusions applied only to spontaneous, rapidly performed movements. [27] Thus, even if we accept the debatable claim that the finger / wrist movements in the Libet experiment were not the result of conscious will, this conclusion cannot automatically be extended to situations for which the term free will would normally be applied.

Another problem is that those who support an anti-free-will interpretation appear to have in mind only rather marginal notions of free will. For example, in a review on the neuroscience of volition, neurobiologist Haggard, a former collaborator of Libet and leading protagonist of the anti-free-will interpretation, mentions the possibility that the brain’s circuits might be influenced by "an unspecified and uncaused cause (the 'will')" . Haggard rejects this view, and concludes the article by stating that "modern neuroscience is shifting towards a view of voluntary action being based on specific brain processes…" . [28] This gives the impression that ‘modern neuroscience’ is gradually triumphing against the illusion of free will, but this is confusing for at least two reasons. First, only a tiny minority of modern philosophers conceive of the will as an ‘uncaused cause’, so why use such a marginal definition? Second, the words about modern neuroscience’s "shifting towards a view of voluntary action being based on specific brain processes" are strange, because this has been the standard view in neuroscience for over half a century. In the same review, Haggard states that the Libet experiment "seems to disprove the everyday concept of 'free will'" ; his reference to ‘everyday concept’ suggests that he recognises that this challenge does not extend to more sophisticated concepts of free will.

Libet’s 1983 experiment reported that brain activity (the RP) reflecting a decision to flex a finger or wrist occurred several hundred milliseconds before the subject became aware of her decision (or urge or will) to move. This has been interpreted, controversially, to suggest that our subjective impression that our conscious wills initiate the movement is illusory. Libet accepted this interpretation, but maintained that conscious will can still play a genuine role in the vetoing of initiated acts.

Many neuroscientists and most philosophers contest the claims about the supposed inefficacy of conscious will, and this paper summarises their arguments. At the neurophysiological level, it has not been shown convincingly that a neural ‘decision’ sufficient to cause the movement occurs before the time of awareness of the decision to move. Even if this could be shown, it would not undermine the conceptions of free will that are defended by most philosophers.

Acknowledgments

The author is grateful to Martyn Frame and Stuart Judge for their helpful comments on an earlier draft of this paper.

[1] Libet, B., Gleason, C.A., Wright, E.W. & Pearl, D.K. ‘Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act’, Brain (1983) 106: 623- 642. [2] Green, J.B. Body, Soul and Human Life: The Nature of Humanity in the Bible , Carlisle: Paternoster (2008). [3] Farrer, A. The Freedom of the Will , London: A & C Black (1958), p.87. [4] Goetz, S. and Taliaferro, C. A Brief History of the Soul , Chichester, UK: Wiley-Blackwell (2011). [5] Nagel, T. The View From Nowhere , Oxford: Oxford University Press (1986), chap.3, p.28; Jeeves, M. & Brown, W.S. Neuroscience, Psychology and Religion , West Conshohocken, PA: Templeton Foundation Press (2009). [6] Gomes, G. ‘The timing of conscious experience: a critical review and reinterpretation of Libet's research’, Consciousness & Cognition (1998) 7: 559-595. [7] Desmurget, M., Reilly, K.T., et al. ‘Movement intention after parietal cortex stimulation in humans’, Science (2009) 324, 811-813. [8] Kornhuber, H.H. and Deecke, L. ‘Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale‘, Pflügers Archiv (1965) 284: 1-17. [9] Kane, R. The Significance of Free Will , New York / Oxford: Oxford University Press (1996), p.232. [10] Fried, I., Mukamel, R. & Kreiman, G. ‘Internally generated preactivation of single neurons in human medial frontal cortex predicts volition’, Neuron (2011) 69: 548-562. [11] Bayne, T. ‘Libet and the case for free will scepticism’, in Swinburne, R. (ed.) Free Will and Modern Science , Oxford: Oxford University Press (2011). [12] Mele, A. R. Effective Intentions: The Power of Conscious Will , New York / Oxford: Oxford University Press (2009). [13] There is a suitable clock at http://www.informationphilosopher.com/freedom/libet_experiments.html . [14] Danquah, A.N., Farrell, M.J. & O'Boyle, D.J. ‘Biases in the subjective timing of perceptual events: Libet et al. (1983) revisited’, Consciousness & Cognition (2008) 17: 616-627. [15] Dennett, D.C. & Kinsbourne, M. ‘Time and the observer’, Behavioral and Brain Sciences (1992) 15: 183–247. [16] Matsuhashi M. & Hallett, M. ‘The timing of the conscious intention to move’, European Journal of Neuroscience (2008) 28: 2344-2351. [17] Soon, C.S., Brass, M., Heinze, H.J. & Haynes, J.D. ‘Unconscious determinants of free decisions in the human brain’, Nature Neuroscience (2008) 11: 543-545. [18] Roland, P.E., Larsen, B., Lassen, N.A. & Skinhoj, E. ‘Supplementary motor area and other cortical areas in organization of voluntary movements in man’, Journal of Neurophysiology (1980) 43: 118-136. [19] Desmurget et al. op. cit. , (see [7]). [20] Haggard P. & Eimer M. ‘On the relation between brain potentials and the awareness of voluntary movements’, Experimental Brain Research (1999) 126: 128-133. [21] Matsuhashi & Hallett op. cit. , (see [16]). [22] Mele op. cit. , (see [12]). [23] Herrmann, C.S., Pauen, M., Min, B.K., Busch, N.A. & Rieger, J.W. ‘Analysis of a choice-reaction task yields a new interpretation of Libet's experiments’, International Journal of Psychophysiology (2008) 67, 151-157. [24] Trevena, J. & Miller, J. ‘Brain preparation before a voluntary action: evidence against unconscious movement initiation’, Consciousness & Cognition (2010) 19, 447-456. [25] Schurger, A., Sitt, J.D. & Dehaene, S. ‘An accumulator model for spontaneous neural activity prior to self-iniated movement’, Proceedings of the National Academy of Sciences . USA doi:10.1073/pnas.1210467109 (2012). [26] Libet, B. Mind Time , Cambridge Mass. / London, UK: Harvard University Press (2004). [27] Libet et al. op. cit. , (see [1]). [28] Haggard, P. ‘Human volition: towards a neuroscience of will’, Nature Reviews Neuroscience (2008) 9: 934-946.

The Libet experiment and its implications for conscious will FARADAY PAPER NO 17

© 2013 The Faraday Institute for Science and Religion This article is Faraday Paper No. 17 and appears on bethinking by the kind permission of the author and the Faraday Institute .

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Peter G.H. Clarke

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“ Philosophy may in no way interfere with the actual use of language; it can in the end only describe it … it leaves everything as it is. ” — L. Wittgenstein.

Am I writing this piece because I am consciously willing or am I just the vehicle of inevitable natural forces and laws that, given my current context as well as biological and social backgrounds, compel me unconsciously to write down this essay? For centuries, such questions have occupied theologians, philosophers, and scientists alike. In the early 1980s, the neurologist Benjamin Libet performed landmark experiments aimed at investigating the role of consciousness in the generation of a motor action ( Libet et al., 1983 ). Libet et al. (1983 ) measured the time when subjects became consciously aware of the decision to move. Using a clock with a rapidly rotating dot, the subjects were asked to note the position of the moving dot when he/she was aware of the conscious decision to move a finger ( Fig. 1 ). Scalp EEG was used simultaneously to monitor brain activity during the experiment. Libet et al. (1983 ) found a premovement buildup of electrical potential called readiness potential (RP) starting ∼550 ms before the movement. Unexpectedly, the conscious awareness of the decision or “the urge to move” emerged only 200 ms before movement, leaving therefore a time lag of ∼350 ms between the initial rising of the RP and the conscious awareness of the decision to flex ( Fig. 1 ). Libet et al. (1983 ) interpreted the early rise in the RP as a reflexion of neuronal computation that unconsciously prepare for the voluntary action. The conscious will emerging at ∼−200 ms could either allow or block the volitional process to go to completion, resulting, respectively, in the execution or withholding of the motor act ( Libet et al., 1983 ). Therefore, according to Libet et al. (1983 ), our brain unconsciously plans our behavior but allows for a conscious “veto” to alter the outcome of our volition. The findings of Libet et al. (1983 ) have had an unrivalled influence on the prevailing view that both our conscious will and subsequent actions are caused by prior neural activity. Recent studies, however, have falsified the causal assumption behind the RP and fine-tuned the notion and the possibility of a volitional “veto.”

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Neuronal basis of RP. Because premovement building of the RP both at the EEG ( a ) ( Libet et al., 1983 ) and single-unit ( b ) ( Fried et al., 2011 ) levels precedes the emergence of the intention to act, it was originally considered to reflect causal and subconscious neuronal preparation of the action. Emmons et al. (2017 ) suggested that such ramping activity encodes time intervals. Recent studies have revealed dopamine as a potential neuromodulatory system mediating the encoding of time intervals as well as action-related cognitive processes through similar ramping patterns of activity ( c ) ( Soares et al., 2016 ; Howard et al., 2017 ; Kim et al., 2017 ).

Two questions directly linked to the conclusions of Libet et al. (1983 ) are central in understanding the relationship between the RP and the conscious agency of our actions. First, what kind of information does RP neurally encode? And second, is the RP causally linked with the behavioral outcome? Within the context of the experiment by Libet et al. (1983 ), the main limitation in understanding the meaning of RP is the concomitant modulation of several factors during the execution of the action. These include action preparation, general anticipation of the occurrence of an action, variable waiting time intervals between the onset and the end of the experiment, choice of whether and when to move, and the impulsive urge to move ( Mele, 2017 ). All these factors could be potentially reflected in the RP. In a recent study published in The Journal of Neuroscience , Emmons et al. (2017 ) conducted elegant behavioral and electrophysiological experiments to show that the potential underlying neuronal correlates of the RP encode the temporal component of action control.

Although the RP described by Libet et al. (1983 ) was recorded at the level of the EEG, the results were replicated at the single-neuron level in human MFC ( Fried et al. 2011 ). At the single-cell level, RP reflects an average signal from two populations of neurons with increasing and decreasing patterns of neuronal firing ( Fried et al., 2011 ). Given the functional homology of the frontal cortex between humans and rodents ( Barthas and Kwan, 2017 ), Emmons et al. (2017 ) recorded single-cell activity from MFC of rats engaged in a behavioral task involving computation of interval timing ( Emmons et al., 2017 , their Fig. 2). Rats were trained to press a lever either 3 or 12 s after the onset of an instructional cue in exchange for a reward. Like the up and down ramping patterns of neuronal activity described in human MFC ( Fried et al., 2011 ), Emmons et al. (2017 ) found two populations of neurons with, respectively, increasing and decreasing neuronal firing rates across time ( Emmons et al., 2017 , their Fig. 3). Importantly, the authors showed that the ramping of neuronal activity followed similar patterns during trials with 3 and 12 s waiting intervals, but the ramping scaled differently to represent elapsed time ( Emmons et al., 2017 , their Figs. 3, 7). These results demonstrate that the premovement ramping of neuronal activity in the MFC encodes temporal processing during the execution of a behavioral action. To further confirm this conclusion, Emmons et al. (2017 ) used a naive Bayesian model to predict time from firing rates of ramping neurons ( Emmons et al., 2017 , their Fig. 8). Emmons et al. (2017 ) found that the pattern of neuronal activity in the MFC predicted time of waiting intervals with a high degree of accuracy ( Emmons et al., 2017 , their Fig. 8). These results explain why Fried et al. (2011 ) found that the ramping rate in MFC was better able to predict the timing of a voluntary decision to move relative to the decision to move alone (98% vs 80%, respectively). Together, these results provide evidence that premovement ramping activity is a key neuronal signal for processing temporal information within the MFC.

In line with other studies showing the involvement of several cortical and subcortical structures in tracking time intervals ( Bhattacharjee, 2006 ), Emmons et al. (2017 ) found that neurons in the dorsomedial striatum also encode waiting time intervals through up and down ramping activity ( Emmons et al., 2017 ). What could be the common underlying neuromodulatory system behind the time-related modulation of neuronal activity in these areas? Both MFC and dorsomedial striatum are densely innervated by midbrain dopaminergic neurons, and three recent studies have directly implicated DA in the control of judgment and estimation of time ( Soares et al., 2016 ; Howard et al., 2017 ; Kim et al., 2017 ). Soares et al. (2016 ) measured and manipulated DA neurons in mice trained, as in the Emmons et al. (2017 ) study, to perform a behavioral task in which they have to estimate the duration of time intervals. In addition to showing that DA neurons encode information about trial-to-trial variability in time estimates, the authors found that pharmacogenetics and optogenetic manipulation of DA neurons were sufficient to slow down or speed up time estimation ( Soares et al., 2016 ). Conversely, depletion of DA in the MFC has been shown to impair temporal control of action ( Kim et al., 2017 ). Interestingly, optogenetic stimulation of pyramidal neurons expressing Type 1 DA receptors compensates for interval timing deficits by normalizing the ramping patterns of neuronal activity in the MFC ( Kim et al., 2017 ). These results corroborate and extend the last experiment performed by Emmons et al. (2017 ) showing the critical role of MFC in encoding and conveying temporal information to striatal neurons ( Emmons et al., 2017 , their Fig. 11). In the third study implicating dopamine in time estimation, Howard et al. (2017 ) used an operant behavioral task in which mice were trained to track time intervals (2 or 8 s and 4 or 16 s) and found that both activity of DA neurons and DA concentration in the dorsal striatum displayed increasing and decreasing ramping patterns that scaled with interval duration. In this study, however, DA signaling did not simply reflect timing or even reward prediction or value alone. Rather, changes in the pattern of DA were associated with internal processes of choice and action selection ( Howard et al., 2017 ). Collectively, all these studies point to the ramping DA signal ( Howe et al., 2013 ) as a potential neuromodulatory system underlying the encoding of interval timing estimation and cognitive processes of action selection by MFC.

What kind of action-related cognitive processes are encoded in the ramping neuronal activity of the MFC? This question brings us back to the question of causality between RP and the behavioral outcome. Originally, Libet et al. (1983 ) interpreted the RP as representing the brain decision “to initiate or, at least, prepare to initiate the act at a time before there is any reportable subjective awareness that such a decision has taken place.” According to this model, once the ramping activity in the frontal cortex reaches a threshold, the motor command is inevitably executed ( Libet et al., 1983 ; Fried et al., 2011 ). Using slightly modified versions of Libet et al. (1983 ) experiment, two recent studies have challenged this interpretation ( Alexander et al., 2016 ; Schultze-Kraft et al., 2016 ). The first demonstrated that humans can still cancel the initiation of a movement, even after the onset of the RP up to a point of no return ∼200 ms before movement onset. Importantly however, it was found that, even after the onset of the movement, it is still possible to alter and abort the movement as it unfolds ( Schultze-Kraft et al., 2016 ). Alexander et al. (2016 ) revealed that robust RPs occur, even in the absence of movement. Together, these two studies demonstrate that premovement RP is not sufficient for the enactment of a motor action. Therefore, the RP must encode processes other than motor-action preparation. Results from Emmons et al. (2017 ) suggest that such ramping activity encodes self-monitored time intervals. This hypothesis is particularly pertinent given that self-monitoring of the passing of time by the experimental subjects is intrinsic to the Libet et al. (1983 ) experiment. Alternatively, although not mutually exclusive, RP might reflect general anticipation (i.e., the conscious experience that an event will soon occur) ( Alexander et al., 2016 ) or simply background neuronal noise ( Schurger et al., 2016 ). Future studies are needed to test these alternatives.

Although the philosophical implications of these results are open for debate, neural determinism defined as the mediation of all mental states by brain processes is the inevitable paradigm, even if we assume the centrality of conscious awareness in action control. This view, however, remains compatible with both physicalism (i.e., all mental states are caused by brains) and interactionism (i.e., brain and mind, while distinct and independent, exert causal effects on one another). This makes the philosophical debate about free will and determinism in a state of underdetermination by current neuroscientific findings. Consequently, and referring to the quotation that started this essay, we might conclude by saying that: Neuroscience may in no way interfere with our first-person experience of the will, it can in the end only describe it … it leaves everything as it is .

Editor's Note: These short reviews of recent JNeurosci articles, written exclusively by students or postdoctoral fellows, summarize the important findings of the paper and provide additional insight and commentary. If the authors of the highlighted article have written a response to the Journal Club, the response can be found by viewing the Journal Club at www.jneurosci.org . For more information on the format, review process, and purpose of Journal Club articles, please see http://jneurosci.org/content/preparing-manuscript#journalclub .

This work was supported by European Community's Marie Sklodowska-Curie IEF Programme Contract 655135 (The Role of Dopamine in the Regulation of Sleep and Circadian Rhythms; CIRCADOPAMINE).

The authors declare no competing financial interests.

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• Author Response to Fifel Journal Club Eric B. Emmons , Benjamin J. De Corte , Youngcho Kim , Krystal L. Parker , Matthew S. Matell and Nandakumar S. Narayanan Published on: 24 January 2018
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A Fresh Look at Free Will: Challenging the Libet Paradigm

Summary: A recent study challenges the long-standing Libet paradigm about free will.

The team discovered that the EEG activity, dubbed readiness potential, registered before decision-making in Libet’s original experiment has no direct correlation to the actual decision.

Moreover, the study revealed that the moment of conscious intention can be influenced by experimental procedures. This ground-breaking research suggests that the Libet paradigm may not be the definitive answer to the complex question of human free will.

• The new research disputes the link between readiness potential and conscious decision-making previously established by Benjamin Libet.
• The study found that experimental procedures could impact the timing of conscious intention awareness.
• The researchers suggest that the Libet paradigm may not be suitable for assessing the concept of free will.

Source: HSE

The dispute about how much free will people have in making their decisions has been going for decades. Neuroscientists have joined this discussion thanks to the electroencephalographic (EEG) experiments of Benjamin Libet.

In the 1970-1980s, he showed that 0.5–1.5 seconds before conscious awareness of the intention to perform a movement, subjects emit EEG activity that predicts this movement.

It turns out that the brain makes a decision and sends readiness potential before a person realizes it, and our actions are nothing more than the result of an unconscious physiological process in the brain .

The results of Libet’s experiments have generated a lot of controversy about free will, and some neurophysiologists have even concluded that it does not exist.

Moreover, Libet’s experiment has been repeated using functional magnetic resonance imaging, and it turns out that the decision of the subject can be predicted even 6-10 seconds before their conscious awareness of it.

The staff of the HSE Institute for Cognitive Neuroscience questioned this experimental paradigm and in their new study confirmed that the time of intention awareness in Libet’s experiments was determined incorrectly.

In addition, EEG activity, or the brain signal indicating the readiness of a decision, which was recorded by Benjamin Libet before the decision was made, actually has no direct link to this decision.

In the Libet’s original experiment, the subjects were asked to occasionally bend their wrists and at the same time remember the moment when they felt ready to perform this action.

The time of intention awareness was recorded from the words of the subjects themselves: they observed a point that moved along the screen-dial, similar to a clock hand, and indicated the position of the point when they felt the desire to bend their hand.

The moment of the final decision was determined by the exact reading of the sensor attached to the wrist of the subjects.

The HSE neuroscientists repeated the experiment with two groups of subjects, adding small changes to the task in one of the groups. Using behavioral reports and hypersensitive EEG techniques, the scientists investigated the correlation between the time of intention awareness and the time of final decision.

It turned out that the time of awareness can be influenced by experimental procedures: for example, without certain training, the subjects are barely able to determine their intentions, and the traditional Libet paradigm pushes them to the feeling that they can determine the moment of decision-making and intention.

Apparently, the instruction itself in the Libet task makes the participants feel that the intention should emerge long before the final decision is made.

In addition, the study confirmed that there is no direct link between the activity of the brain preceding the action and the intention to perform the action. The sense of intention emerged in the subjects at different points in time, whereas the readiness potential was always registered at about the same time.

Thus, the readiness potential may reflect the general dynamics of the decision-making process about making a move, but it does not mean that the intention to act has already been generated.

“Our study highlights the ambiguity of Libet’s research and proves the absence of a direct correlation between the brain signal and decision-making.

“It appears that the classical Libet paradigm is not suitable for answering the question of whether we have free will while making decisions. We need to come up with a new approach to this extremely interesting scientific puzzle,” says Dmitry Bredikhin, author of the research, Junior Research Fellow at the Centre for Cognition & Decision Making.

“Neuroscience tries to answer key questions in our life, including questions of free will and responsibility for our actions. We need to be especially precise in order to draw conclusions that affect our outlook and attitude to life. Therefore, we tried to understand the predetermination of our decisions and confirmed a number of shortcomings in the famous experiments of Benjamin Libet.

“This does not mean that we have closed this issue of the illusory nature of our free will, but rather emphasizes that the discussion continues. This might be one of the most interesting questions in modern science, to which we have yet to give a definitive answer,” comments Vasily Klucharev, Project coordinator, Leading Research Fellow of the Institute for Cognitive Neuroscience.

About this neuroscience and free will research news

Author: Ksenia Bregadze Source: HSE Contact: Ksenia Bregadze – HSE Image: The image is credited to Neuroscience News

Original Research: Open access. “ (Non)-experiencing the intention to move: On the comparisons between the Readiness Potential onset and Libet’s W-time ” by Dmitry Bredikhin et al. Neuropsychologia

(Non)-experiencing the intention to move: On the comparisons between the Readiness Potential onset and Libet’s W-time

A seminal study by Libet et al. (1983) provided a popular approach to compare the introspective timing of movement execution (the M-time) and the intention to move (the W-time) with respect to the onset of the readiness potential (RP).

The difference between the W-time and the RP onsets contributed significantly to the current free-will discussion, insofar as it has been repeatedly shown that the RP onset unequivocally precedes the W-time.

However, the interpretations of Libet’s paradigm continuously attract criticism, questioning the use of both the W-time and the RP onset as indicators of motor intention.

In the current study, we further probe whether the W-time is rather an intention-unrelated product of the participant’s inference than an unambiguous temporal marker of the intention to move.

Using behavioral reports and concurrent multichannel EEG, we investigated the relationship between the W-time and M-time introspective reports in two groups of participants who started an experiment with a series of different reports.

Congruently with previous studies, we have shown that the W-time is affected by the experimental procedures: participants who had prior experience reporting the M-time provided significantly earlier W-time.

However, contrary to previous papers, we revealed that even naive participants do introspectively differentiate the W-time and the M-time, which suggests that the W-time might actually reflect the intention to move, at least to some extent. We, therefore, suggest that training-based modulation of the W-time values may explain this finding.

Moreover, we further confirm the absence of a direct link between the RP onset and the W-time by showing no covariation between them in both experimental groups. In turn, our findings question the overall interpretation of the comparison between these two time points.

Overall, our study further emphasizes the ambiguity of Libet’s paradigm, and suggests that the relatedness of both the RP and the W-time to the movement initiation processes should not be assumed a priori.

I believe we have free will despite large amount of literature around it. Let us take the Libet task. Just ask the volunteer to repeat the task continuously beyond the first M. For example say a person vibrates his fore finger as he pleases. The EEG should show cyclic regular or irregular M kind of movements. There will be no RP expected. Is this not free will of the volunteer? re RP I have a generalist theory which is not easily acceptable. A Sethuramiah

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Readiness potentials preceding spontaneous motor acts: voluntary vs. involuntary control

Affiliation.

• 1 Institute for Medical Psychology, University of Munich, F.R.G.
• PMID: 1699728
• DOI: 10.1016/0013-4694(90)90036-j

Libet et al. (1983) developed a method to compare the onset time of a readiness potential (RP) with the onset time of the corresponding intention to perform a spontaneous voluntary motor act. In relation to the onset of the RP, the time of conscious intention to move followed 350 msec later. From these results Libet (1985) concluded that the cerebral initiation of a spontaneous voluntary act begins unconsciously. We investigated the alternative interpretation that with the instruction to pay attention to feelings of 'wanting to move,' automatic and normally unconscious motor acts might have been brought to a level of conscious awareness. Therefore we conducted 3 kinds of experiment. In the first, RPs were measured from subjects performing unconscious movements. The second experiment was a replication of Libet's study while the third was a resting condition in which subjects looked for intentions to move introspectively. The results showed that RPs beginning approximately 500 msec before movement onset can be obtained with unconsciously as well as consciously performed spontaneous motor acts. The different scalp distributions of the two types of RP indicate that unconscious movements can be attributed to the activation of a contralateral process (lateral premotor system (LPS), primary motor cortex), whereas voluntary spontaneous motor acts seemed to be predominated by the medial premotor system (MPS). It is proposed that in the Libet situation focused attention on internal events led to the conscious detection of a normally unconscious process. This resulted in the activation of the MPS, especially the supplementary motor area (SMA), which released the starting signal for the execution of the motor act. We believe that the activation of the SMA and the urge to move occurred at the same time.

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• Voluntary acts and readiness potentials. Libet B. Libet B. Electroencephalogr Clin Neurophysiol. 1992 Jan;82(1):85-6. doi: 10.1016/0013-4694(92)90186-l. Electroencephalogr Clin Neurophysiol. 1992. PMID: 1370148 No abstract available.

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Exposing some holes in Libet’s classic free will study

Research has found that Libet would have arrived at a different estimate if he’d used a visual or auditory control task to make his adjustment.

19 September 2008

By Christian Jarrett

Benjamin Libet's  classic 1983 experiment purported to show that preparatory brain activity precedes our conscious decision to move – a controversial finding interpreted by some as evidence that free will is illusory.

In Libet's study, participants reported the time on a clock at the instant they had decided to move a finger. This is less straightforward than it sounds. Visual processing is sluggish whereas participants were presumably instantly aware of when they'd made a conscious decision to move. This would have led them to report a decision time that was too early (i.e. at the instant of their decision, the participants' brains would only just have been getting round to processing an earlier time on the clock).

Libet's team realised this, so in a separate control condition they also asked participants to report the timing of an electrical stimulus applied to their hand – the error in this time estimation was then used to apply a correction to participants' estimates of when they'd made a movement decision.

But in a new study, Adam Danquah and colleagues point out that our different sensory modalities operate at different speeds. They copied the control condition of Libet's experimental set-up, but they asked participants to report not just the timing of a mild electric shock, but also of a flash in the centre of the clock, and the sound of a click (delivered through headphones).

The researchers found that the participants' estimates were less accurate (i.e. even earlier) for the visual flash and auditory click than for the electric shock. In other words, Libet would have arrived at a different estimate of when participants had made a decision to move if he'd used a visual or auditory control task to make his adjustment.

"The degree of variability in bias across modalities and studies means that it is very difficult to know what correctional standard, if any, can be applied to awareness times of endogenous events [e.g. decisions]," the researchers wrote.

However, defenders of free-will shouldn't take comfort in these new results. Danquah and his colleagues added an important note about the implications of their work: "the magnitude of the biases reported here suggests that they [Libet's team] underestimated the degree to which… [preparatory brain activity] preceded the intention to move!"

In a second experiment, Danquah and his colleagues also identified another problem with the Libet paradigm. The clock used by Libet featured a dot that circled the clock-face, rather like a second-hand. Danquah's team showed that the speed at which the dot circled the clock face also affected participants' time estimations – the faster the dot, the more accurate participants' estimates became.

"The results reported here have implications for the whole tradition of having participants locate temporally subjective events using the clock paradigm," the researchers concluded.

Further reading

A DANQUAH, M FARRELL, D OBOYLE (2008). Biases in the subjective timing of perceptual events: Libet et al. (1983) revisited Consciousness and Cognition, 17 (3), 616-627 DOI:  10.1016/j.concog.2007.09.005

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