What Is the Readiness Potential?
2021; Elsevier BV; Volume: 25; Issue: 7 Linguagem: Inglês
10.1016/j.tics.2021.04.001
ISSN1879-307X
AutoresAaron Schurger, Pengbo Hu, Joanna Pak, Adina L. Roskies,
Tópico(s)Healthcare Decision-Making and Restraints
ResumoThe readiness potential (RP) has been widely interpreted to indicate preparation for movement and is used to argue that our brains decide before we do. It thus has been a fulcrum for discussion about the neuroscience of free will.Recent computational models provide an alternative framework for thinking about the significance of the RP, suggesting instead that the RP is a natural result of the operation of a stochastic accumulator process of decision-making, analyzed by time-locking to threshold-crossing events.These models call for a reevaluation of: (i) the ontological standing of the RP as reflecting a real, causally efficacious signal in the brain; (ii) the meaningfulness of temporal comparisons between the 'onset' of the RP and the timing of other phenomena; (iii) the moment at which we, as experimenters, identify that a decision to act has been made; and (iv) the relevance of the RP for discussions of free will. The readiness potential (RP), a slow buildup of electrical potential recorded at the scalp using electroencephalography, has been associated with neural activity involved in movement preparation. It became famous thanks to Benjamin Libet (Brain 1983;106:623–642), who used the time difference between the RP and self-reported time of conscious intention to move to argue that we lack free will. The RP's informativeness about self-generated action and derivatively about free will has prompted continued research on this neural phenomenon. Here, we argue that recent advances in our understanding of the RP, including computational modeling of the phenomenon, call for a reassessment of its relevance for understanding volition and the philosophical problem of free will. The readiness potential (RP), a slow buildup of electrical potential recorded at the scalp using electroencephalography, has been associated with neural activity involved in movement preparation. It became famous thanks to Benjamin Libet (Brain 1983;106:623–642), who used the time difference between the RP and self-reported time of conscious intention to move to argue that we lack free will. The RP's informativeness about self-generated action and derivatively about free will has prompted continued research on this neural phenomenon. Here, we argue that recent advances in our understanding of the RP, including computational modeling of the phenomenon, call for a reassessment of its relevance for understanding volition and the philosophical problem of free will. The readiness potential (RP) (see Glossary) or Bereitschaftspotential (BP) is a brain signal linked to voluntary movement. Its existence has been used to argue against the possibility of free will. Originally identified by Kornhuber and Deeke [1.Kornhuber H.H. Deecke L. Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale.Pflugers Arch. 1965; 284: 1-17Crossref Scopus (1119) Google Scholar], the RP emerges from the analysis of electroencephalogram (EEG) data recorded during experimental tasks involving spontaneous or self-paced movements. When EEG traces, recorded during such a task, are time-locked to movement onset and averaged together, a slow negative-going electrical potential is evident leading up to movement onset (Box 1). The RP is prominent at central electrode sites located above mesial motor cortical areas and peaks contralateral to the moving limb. In experiments that average data from multiple subjects making self-paced movements, the RP is highly replicable. The RP has traditionally been interpreted as a sign of planning and preparation for movement and it is well-established as a reliable signal that precedes self-initiated movement in the group average. However, recent literature raises questions about the RP's ontological status as a real signal in the brain, its relation to action, its significance for arguments about volition, and its implications for free will. We review this recent literature and offer a reinterpretation of the nature of the signal that undermines its relevance for classic arguments against free will.Box 1The Readiness Potential, Past and PresentThe empirical literature on the RP is vast and varied and difficult to fit under a single theoretical account. Libet's [2.Libet B. et al.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: 623-642Crossref PubMed Google Scholar] classic study distinguished between two types of RPs: type I RPs, involving 'preplanning', had significantly earlier onsets (approximately 1000 ms prior to movement) than type II RPs, associated with spontaneous movement (approximately 500 ms prior), but cf. [66.Fairhall S.L. et al.Volition and the idle cortex: beta oscillatory activity preceding planned and spontaneous movement.Conscious. Cogn. 2007; 16: 221-228Crossref PubMed Scopus (6) Google Scholar] who found the opposite to be true with a larger cohort of subjects. The RP is commonly characterized as having an early and a late component [29.Shibasaki H. Hallett M. What is the Bereitschaftspotential?.Clin. Neurophysiol. 2006; 117: 2341-2356Crossref PubMed Scopus (684) Google Scholar]. The early component (~1500–400 ms prior to movement onset) is a slow but gradual increase in negativity, symmetrical between the two hemispheres, that has been attributed to activity in the supplementary motor area and premotor cortex, whereas the late component (~400–0 ms) is generated by activity in the primary motor cortex. The spatial focus and amplitude of the RP are dependent on particulars of the experimental task, including movement effector [67.Brunia C.H.M. et al.Movement related slow potentials. II. A contrast between finger and foot movements in left-handed subjects.Electroencephalogr. Clin. Neurophysiol. 1985; 60: 135-145Abstract Full Text PDF PubMed Scopus (28) Google Scholar, 68.Damen E.J. et al.The differential effects of extremity and movement side on the scalp distribution of the readiness potential (RP) and the stimulus-preceding negativity (SPN).Electroencephalogr. Clin. Neurophysiol. 1996; 99: 508-516Abstract Full Text PDF PubMed Scopus (13) Google Scholar, 69.Rektor I. Parallel information processing in motor systems: intracerebral recordings of readiness potential and CNV in human subjects.Neural Plasticity. 2000; 7: 65-72Crossref PubMed Google Scholar], limb dominance [70.Dirnberger G. et al.On the regularity of preparatory activity preceding movements with the dominant and non-dominant hand: a readiness potential study.Int. J. Psychophysiol. 2011; 81: 127-131Crossref PubMed Scopus (6) Google Scholar], attention to timing of movement [71.Baker K.S. et al.Neural activity in readiness for incidental and explicitly timed actions.Neuropsychologia. 2012; 50: 715-722Crossref PubMed Scopus (27) Google Scholar] or the intention to move [72.Takashima S. et al.The volition, the mode of movement selection and the readiness potential.Exp. Brain Res. 2020; 238: 2113-2123Crossref PubMed Scopus (0) Google Scholar], and other task factors [73.Joordens S. et al.When timing the mind one should also mind the timing: biases in the measurement of voluntary actions.Conscious. Cogn. 2002; 11: 231-240Crossref PubMed Scopus (29) Google Scholar,74.Kilner J.M. et al.Motor activation prior to observation of a predicted movement.Nat. Neurosci. 2004; 7: 1299-1301Crossref PubMed Scopus (283) Google Scholar], including possibly beliefs in free will [75.Rigoni D. et al.Inducing disbelief in free will alters brain correlates of preconscious motor preparation: the brain minds whether we believe in free will or not.Psychol. Sci. 2011; 22: 613-618Crossref PubMed Scopus (87) Google Scholar]. Recent work suggests that the RP may be more prominent in arbitrary versus reason-based decisions [65.Maoz U. et al.Neural precursors of decisions that matter—an ERP study of deliberate and arbitrary choice.eLife. 2019; 8e39787Crossref PubMed Scopus (8) Google Scholar].Numerous studies linking the RP to a variety of phenomena and experimental manipulations complicate its interpretation, especially as a phenomenon indicative of volition. For example, the RP may be related to and modulated by anticipation of the sensory and/or somatosensory consequences of the action [76.Reznik D. et al.Predicted sensory consequences of voluntary actions modulate amplitude of preceding readiness potentials.Neuropsychologia. 2018; 119: 302-307Crossref PubMed Scopus (12) Google Scholar,77.Wen W. et al.The readiness potential reflects the reliability of action consequence.Sci. Rep. 2018; 8: 11865Crossref PubMed Scopus (2) Google Scholar] and by awareness of movement intention [78.Takashima S. et al.The effect of conscious intention to act on the Bereitschaftspotential.Exp. Brain Res. 2018; 236: 2287-2297Crossref PubMed Scopus (4) Google Scholar]. Some have suggested that the RP is linked to decision uncertainty [41.Schurger A. An accumulator model for spontaneous neural activity prior to self-initiated movement.Proc. Natl. Acad. Sci. U. S. A. 2012; 109: E2904-E2913Crossref PubMed Scopus (197) Google Scholar,79.Nachev P. et al.Functional role of the supplementary and pre-supplementary motor areas.Nat. Rev. Neurosci. 2008; 9: 856-869Crossref PubMed Scopus (1013) Google Scholar], but at least in one way of operationalizing uncertainty, this is not borne out [80.Travers E. Haggard P. The readiness potential reflects the internal source of action, rather than decision uncertainty.Eur. J. Neurosci. 2020; 53: 1533-1544Crossref PubMed Scopus (0) Google Scholar]. Consistent with other work [65.Maoz U. et al.Neural precursors of decisions that matter—an ERP study of deliberate and arbitrary choice.eLife. 2019; 8e39787Crossref PubMed Scopus (8) Google Scholar], it appears to be associated more with endogenous than external cues [80.Travers E. Haggard P. The readiness potential reflects the internal source of action, rather than decision uncertainty.Eur. J. Neurosci. 2020; 53: 1533-1544Crossref PubMed Scopus (0) Google Scholar]. The RP is diminished in amplitude or absent with cerebellar lesions [81.Kitamura J. et al.Cortical potentials preceding voluntary finger movement in patients with focal cerebellar lesion.Clin. Neurophysiol. 1999; 110: 126-132Crossref PubMed Scopus (23) Google Scholar] and diminished by damage to the prefrontal cortex [82.Wiese H. Impaired movement-related potentials in acute frontal traumatic brain injury.Clin. Neurophysiol. 2004; 115: 289-298Crossref PubMed Scopus (35) Google Scholar] and in neuropsychiatric conditions such as Parkinson's disease [83.Jahanshahi M. et al.Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects.Brain. 1995; 118: 913-933Crossref PubMed Google Scholar] and obsessive compulsive disorder (OCD) [84.Takashima S. et al.Disruption of volitional control in obsessive-compulsive disorder: evidence from the Bereitschaftspotential.Psychiatry Res. Neuroimaging. 2019; 290: 30-37Crossref PubMed Scopus (3) Google Scholar]. It is unclear whether or not the (seemingly involuntary) tics of Tourette's patients are preceded by an RP [85.Mainka T. et al.Learning volition: a longitudinal study of developing intentional awareness in Tourette syndrome.Cortex. 2020; 129: 33-40Crossref PubMed Scopus (1) Google Scholar]. The breathing cycle, a largely involuntary phenomenon, has been linked to a modulation in the amplitude of the RP [86.Park H.-D. et al.Breathing is coupled with voluntary action and the cortical readiness potential.Nat. Commun. 2020; 11: 289Crossref PubMed Scopus (8) Google Scholar]. However, because breathing strongly influences the onset time of spontaneous voluntary movement [86.Park H.-D. et al.Breathing is coupled with voluntary action and the cortical readiness potential.Nat. Commun. 2020; 11: 289Crossref PubMed Scopus (8) Google Scholar], it is difficult to determine whether these observations reflect a causal relationship or an incidental one. The empirical literature on the RP is vast and varied and difficult to fit under a single theoretical account. Libet's [2.Libet B. et al.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: 623-642Crossref PubMed Google Scholar] classic study distinguished between two types of RPs: type I RPs, involving 'preplanning', had significantly earlier onsets (approximately 1000 ms prior to movement) than type II RPs, associated with spontaneous movement (approximately 500 ms prior), but cf. [66.Fairhall S.L. et al.Volition and the idle cortex: beta oscillatory activity preceding planned and spontaneous movement.Conscious. Cogn. 2007; 16: 221-228Crossref PubMed Scopus (6) Google Scholar] who found the opposite to be true with a larger cohort of subjects. The RP is commonly characterized as having an early and a late component [29.Shibasaki H. Hallett M. What is the Bereitschaftspotential?.Clin. Neurophysiol. 2006; 117: 2341-2356Crossref PubMed Scopus (684) Google Scholar]. The early component (~1500–400 ms prior to movement onset) is a slow but gradual increase in negativity, symmetrical between the two hemispheres, that has been attributed to activity in the supplementary motor area and premotor cortex, whereas the late component (~400–0 ms) is generated by activity in the primary motor cortex. The spatial focus and amplitude of the RP are dependent on particulars of the experimental task, including movement effector [67.Brunia C.H.M. et al.Movement related slow potentials. II. A contrast between finger and foot movements in left-handed subjects.Electroencephalogr. Clin. Neurophysiol. 1985; 60: 135-145Abstract Full Text PDF PubMed Scopus (28) Google Scholar, 68.Damen E.J. et al.The differential effects of extremity and movement side on the scalp distribution of the readiness potential (RP) and the stimulus-preceding negativity (SPN).Electroencephalogr. Clin. Neurophysiol. 1996; 99: 508-516Abstract Full Text PDF PubMed Scopus (13) Google Scholar, 69.Rektor I. Parallel information processing in motor systems: intracerebral recordings of readiness potential and CNV in human subjects.Neural Plasticity. 2000; 7: 65-72Crossref PubMed Google Scholar], limb dominance [70.Dirnberger G. et al.On the regularity of preparatory activity preceding movements with the dominant and non-dominant hand: a readiness potential study.Int. J. Psychophysiol. 2011; 81: 127-131Crossref PubMed Scopus (6) Google Scholar], attention to timing of movement [71.Baker K.S. et al.Neural activity in readiness for incidental and explicitly timed actions.Neuropsychologia. 2012; 50: 715-722Crossref PubMed Scopus (27) Google Scholar] or the intention to move [72.Takashima S. et al.The volition, the mode of movement selection and the readiness potential.Exp. Brain Res. 2020; 238: 2113-2123Crossref PubMed Scopus (0) Google Scholar], and other task factors [73.Joordens S. et al.When timing the mind one should also mind the timing: biases in the measurement of voluntary actions.Conscious. Cogn. 2002; 11: 231-240Crossref PubMed Scopus (29) Google Scholar,74.Kilner J.M. et al.Motor activation prior to observation of a predicted movement.Nat. Neurosci. 2004; 7: 1299-1301Crossref PubMed Scopus (283) Google Scholar], including possibly beliefs in free will [75.Rigoni D. et al.Inducing disbelief in free will alters brain correlates of preconscious motor preparation: the brain minds whether we believe in free will or not.Psychol. Sci. 2011; 22: 613-618Crossref PubMed Scopus (87) Google Scholar]. Recent work suggests that the RP may be more prominent in arbitrary versus reason-based decisions [65.Maoz U. et al.Neural precursors of decisions that matter—an ERP study of deliberate and arbitrary choice.eLife. 2019; 8e39787Crossref PubMed Scopus (8) Google Scholar]. Numerous studies linking the RP to a variety of phenomena and experimental manipulations complicate its interpretation, especially as a phenomenon indicative of volition. For example, the RP may be related to and modulated by anticipation of the sensory and/or somatosensory consequences of the action [76.Reznik D. et al.Predicted sensory consequences of voluntary actions modulate amplitude of preceding readiness potentials.Neuropsychologia. 2018; 119: 302-307Crossref PubMed Scopus (12) Google Scholar,77.Wen W. et al.The readiness potential reflects the reliability of action consequence.Sci. Rep. 2018; 8: 11865Crossref PubMed Scopus (2) Google Scholar] and by awareness of movement intention [78.Takashima S. et al.The effect of conscious intention to act on the Bereitschaftspotential.Exp. Brain Res. 2018; 236: 2287-2297Crossref PubMed Scopus (4) Google Scholar]. Some have suggested that the RP is linked to decision uncertainty [41.Schurger A. An accumulator model for spontaneous neural activity prior to self-initiated movement.Proc. Natl. Acad. Sci. U. S. A. 2012; 109: E2904-E2913Crossref PubMed Scopus (197) Google Scholar,79.Nachev P. et al.Functional role of the supplementary and pre-supplementary motor areas.Nat. Rev. Neurosci. 2008; 9: 856-869Crossref PubMed Scopus (1013) Google Scholar], but at least in one way of operationalizing uncertainty, this is not borne out [80.Travers E. Haggard P. The readiness potential reflects the internal source of action, rather than decision uncertainty.Eur. J. Neurosci. 2020; 53: 1533-1544Crossref PubMed Scopus (0) Google Scholar]. Consistent with other work [65.Maoz U. et al.Neural precursors of decisions that matter—an ERP study of deliberate and arbitrary choice.eLife. 2019; 8e39787Crossref PubMed Scopus (8) Google Scholar], it appears to be associated more with endogenous than external cues [80.Travers E. Haggard P. The readiness potential reflects the internal source of action, rather than decision uncertainty.Eur. J. Neurosci. 2020; 53: 1533-1544Crossref PubMed Scopus (0) Google Scholar]. The RP is diminished in amplitude or absent with cerebellar lesions [81.Kitamura J. et al.Cortical potentials preceding voluntary finger movement in patients with focal cerebellar lesion.Clin. Neurophysiol. 1999; 110: 126-132Crossref PubMed Scopus (23) Google Scholar] and diminished by damage to the prefrontal cortex [82.Wiese H. Impaired movement-related potentials in acute frontal traumatic brain injury.Clin. Neurophysiol. 2004; 115: 289-298Crossref PubMed Scopus (35) Google Scholar] and in neuropsychiatric conditions such as Parkinson's disease [83.Jahanshahi M. et al.Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects.Brain. 1995; 118: 913-933Crossref PubMed Google Scholar] and obsessive compulsive disorder (OCD) [84.Takashima S. et al.Disruption of volitional control in obsessive-compulsive disorder: evidence from the Bereitschaftspotential.Psychiatry Res. Neuroimaging. 2019; 290: 30-37Crossref PubMed Scopus (3) Google Scholar]. It is unclear whether or not the (seemingly involuntary) tics of Tourette's patients are preceded by an RP [85.Mainka T. et al.Learning volition: a longitudinal study of developing intentional awareness in Tourette syndrome.Cortex. 2020; 129: 33-40Crossref PubMed Scopus (1) Google Scholar]. The breathing cycle, a largely involuntary phenomenon, has been linked to a modulation in the amplitude of the RP [86.Park H.-D. et al.Breathing is coupled with voluntary action and the cortical readiness potential.Nat. Commun. 2020; 11: 289Crossref PubMed Scopus (8) Google Scholar]. However, because breathing strongly influences the onset time of spontaneous voluntary movement [86.Park H.-D. et al.Breathing is coupled with voluntary action and the cortical readiness potential.Nat. Commun. 2020; 11: 289Crossref PubMed Scopus (8) Google Scholar], it is difficult to determine whether these observations reflect a causal relationship or an incidental one. The RP gained notoriety largely due to the work of Benjamin Libet in the 1980s [2.Libet B. et al.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: 623-642Crossref PubMed Google Scholar]. Libet asked subjects to spontaneously and repeatedly perform a simple movement, flexion of the fingers and/or wrist, while he measured EEG activity and electromyography (EMG) from the relevant muscles. Subjects also monitored a rapidly rotating clock dial and were told to note, for each movement, the time on the clock at which they first felt the urge, or will, to move (W-time). Their retrospective reports enabled Libet to establish a temporal relationship between a subject's self-reported awareness of willing to move, the time of movement, and the onset of the RP. The results are familiar to many even outside of neuroscience: average W-time is only approximately 200 ms before movement onset, hundreds of ms after the apparent onset of the RP. Libet correctly reasoned that if subjects consciously willed themselves to move after the brain began preparing to move, conscious will could not cause the RP's initiation. Given the RP's perceived status as a preparatory signal to move, he further reasoned that the subjects' brains had already unconsciously initiated movement before their conscious willing. As he put it: '…the brain evidently "decides" to initiate or, at the least, prepares to initiate the act at a time before there is any reportable subjective awareness that such a decision has taken place. It is concluded that cerebral initiation even of a spontaneous voluntary act, of the kind studied here, can and usually does begin unconsciously…These considerations would appear to introduce certain constraints on the potential of the individual for exerting conscious initiation and control over his voluntary acts.' [2.Libet B. et al.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: 623-642Crossref PubMed Google Scholar]. Since many believe that conscious initiation and control over one's voluntary acts are required for free will, Libet's work was widely interpreted as undermining the possibility of free will [3.Sinnott-Armstrong W. Nadel L. Conscious Will and Responsibility. Oxford University Press, 2011Google Scholar, 4.Schlosser M.E. Free will and the unconscious precursors of choice.Philos. Psychol. 2012; 25: 365-384Crossref Scopus (13) Google Scholar, 5.Harris S. Free Will. Free Press, 2012Google Scholar, 6.Racine E. et al.Media portrayal of a landmark neuroscience experiment on free will.Sci. Eng. Ethics. 2017; 23: 989-1007Crossref PubMed Scopus (10) Google Scholar, 7.Saigle V. et al.The impact of a landmark neuroscience study on free will: a qualitative analysis of articles using Libet and colleagues' methods.AJOB Neurosci. 2018; 9: 29-41Crossref Scopus (18) Google Scholar, 8.Coyne J. Why you don't really have free will.USA Today. 2012; (Published online January 1, 2012. http://www.thinking-differently.com/phil001/wp-content/uploads/2013/03/Readings_free_will.pdf)Google Scholar]. Libet himself recognized at least two ways his stark conclusions negating free will were limited. First, he postulated that we could veto our brain's unconscious decisions in the period between when we became aware of our intention to move and the movement itself; this veto power is commonly referred to as 'free won't' [9.Ramachandran V.S. The zombie within.New Sci. 1998; 2150: 32Google Scholar]. Subsequent studies have shown that such conscious veto decisions are also preceded by an RP and thus subject to the same problematic delay before W-time, making such a position seem untenable [10.Trevena J. Miller J. 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This also makes 'free won't' seem untenable, because the window of time in which Libet suggested subjects could veto a movement begins precisely when subjects can no longer veto a movement. More helpfully, Libet suggested that many of our actions result from conscious deliberation that unfolds over much longer time-scales [2.Libet B. et al.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: 623-642Crossref PubMed Google Scholar], which would not be subject to these timing issues. Indeed, philosophers have argued that few of the decisions for which responsibility (and thus free will) is of concern fit the profile of Libet-style tasks [14.Mele A.R. Effective Intentions: The Power of Conscious Will. Oxford University Press, 2009Crossref Scopus (242) Google Scholar, 15.Bok H. Freedom and Responsibility. 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There's no such thing as free will but we're better off believing in it anyway.The Atlantic. 2016; (Published online June 2016. https://www.theatlantic.com/magazine/archive/2016/06/theres-no-such-thing-as-free-will/480750/)Google Scholar, 26.Goleman D. The New York Times 7 Feb, Section C, p. 1.1984Google Scholar, 27.Johnson G. The New York Times 3 May, Section 7, p. 34.1998Google Scholar] with little critical commentary. Recent fMRI evidence showing that free decisions can be predicted several seconds before the choice is made [22.Soon C.S. et al.Unconscious determinants of free decisions in the human brain.Nat. Neurosci. 2008; 11: 543-545Crossref PubMed Scopus (854) Google Scholar,28.Soon C.S. et al.Predicting free choices for abstract intentions.Proc. Natl. Acad. Sci. U. S. A. 2013; 110: 6712-6722Crossref PubMed Scopus (105) Google Scholar] has helped to cement this view. Note, however, that although prediction accuracy was statistically significantly above chance, it was still only marginally better than a random guess. Because of the dramatic conclusions drawn from Libet's work, the RP continues to be a topic of interest in the brain sciences, including among neurologists. Research o
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