EEG activations during intentional inhibition of voluntary action: An electrophysiological correlate of self-control?
Introduction
The ability to make voluntary actions is a defining human characteristic. A widely accepted definition characterises voluntary actions as being internally generated; specified by a person's decisions and intentions rather than by external stimuli. An important aspect of voluntary action is the decision not to act. This decision can take two forms. First, one might decide not to begin any action preparation at all, but remain in an inactive state. Second, one might prepare an action, but subsequently make a deliberate decision to inhibit the execution of the action. Respectively, these have been called “early” and “late” decisions about whether to act (Haggard, 2008). Here we concentrate on the second “late” form, involving the decision to inhibit an action for which the neural preparation has already begun. Such internal inhibition could prevent us from inappropriately and automatically reacting to environmental stimuli, for example when suppressing the urge to utter an inappropriate remark that may arrive uninvited on the tip of our tongue in a social situation. Concepts of action responsibility point out that we are responsible for our actions because we could have decided to withhold them (Dennett, 1984). Inhibition has also played a key role in recent debates about the nature of volition. Materialist neuroscience holds that conscious intention (“urge”) is a consequence of unconscious preparatory brain activity. Libet (1999) suggested that conscious will may nevertheless influence our actions through a second mechanism of “conscious veto” occurring between the awareness of intention and the onset of movement. This view replaces free will with “free won’t” (Obhi & Haggard, 2004). However, the theoretical objections to conscious causation that apply to the case of free will apply equally to “free won’t”.
Here we set aside philosophical considerations, and consider the process of intentional inhibition itself. The experience of deciding to withhold an action at the last moment is recognised by many people. However, studies of last-moment inhibitory control generally involve external stop-signals (e.g. De Jong et al., 1995, Logan et al., 1984) rather than internal decisions. In these paradigms, participants respond to ‘Go’ stimuli but are required to inhibit their response if a ‘NoGo’ or ‘stop-’ signal is delivered. These studies suggest a specific cognitive function of externally driven inhibition, localised to right inferior frontal cortex (Aron et al., 2003, Aron and Poldrack, 2006, Chambers et al., 2006, Verbruggen and Logan, 2008).
Intentional inhibition involves an internal decision to stop at the last moment, rather than a response to an external stop-signal. Although this form of inhibition is clearly relevant to responsibility for action, it has been largely ignored in the experimental literature, perhaps because it is hard to study. In particular, an intentional action that is intentionally inhibited has no imperative stimulus, and no behavioural output. Therefore, there is no overt marker for the neural processes being studied. Recently, Brass and Haggard (2007) developed a method of studying intentional inhibition based on subjective markers. Participants freely decided when to press a key, but were also instructed to withhold the keypress at the last possible moment on some trials. That is, they were instructed to reproduce on every trial the decision process between action and inhibition that we recognise from key moments of everyday life. Using Libet's clock method, participants reported the exact moment when they experienced the urge to press the key (Libet's “W judgement”) even on trials where they inhibited the overt movement itself. Thus, the subjective experience of conscious intention provided a temporal marker for comparing fMRI activations on trials where participants prepared but then intentionally inhibited actions to activations on trials where they prepared and then executed actions. Intentional inhibition was specifically associated with activation of an area of left fronto-median cortex. Although these conclusions, and the present paper, depend on Libet et al.’s (Libet, Gleason, Wright, & Pearl, 1983) method, they do not require all the assumptions about the source of voluntary action that characterise the ‘free will’ debate. Specifically, the experimental logic requires only that people have temporally specific conscious experiences during the generation of endogenous actions, that these experiences are related to specific brain processes, and that the experience and the brain processes occur after the onset of action preparation but prior to a ‘point of no return’ for action execution.
However, the poor temporal resolution of fMRI means that such methods cannot clearly identify when the putative inhibitory processes occurred. Indeed, timing is crucial to identifying the process at all: the last-moment intentional inhibition of interest here should occur after action preparation but before execution. Timing information is required to distinguish inhibition from other related events, such as the feeling of frustration (Abler, Walter, & Erk, 2005) associated with failing to complete actions. EEG, in contrast, has excellent temporal resolution. It has been used extensively to investigate both action preparation processes (Pfurtscheller, 1992), and external stop-signal inhibition (De Jong et al., 1995). Few previous studies have investigated the EEG correlates of intentional inhibition, but Hummel, Andres, Altenmüller, Dichgans, and Gerloff (2002) observed focal increases of oscillatory alpha activity over sensorimotor areas when a novel task context required participants to tonically inhibit previously acquired sensorimotor associations. Serrien, Orth, Evans, Lees, and Brown (2005) reported increased coherence between frontal and motor cortices during voluntary suppression of motor tics in patients with Tourette's syndrome.
Here, we used EEG frequency analysis to investigate the processes of intentional inhibition when participants were instructed to prepare and then cancel a voluntary action. A subjective marker (W judgement) was used to align recordings. Because W judgements are quite variable, the chances of detecting any event-related potential (ERPs) corresponding to inhibition could be low. However, event-related changes in EEG spectral power may occur over longer time scales than many ERPs, and have a better signal-to-noise ratio (Pfurtscheller, 1992). Event-related desynchronisation (ERD) of upper alpha- and lower beta-band rhythms (8–24 Hz) is associated with motor preparation and execution. Movement termination is followed by an increased synchronisation (ERS; Pfurtscheller & da Silva, 1999), or post-movement “beta rebound”, presumably reflecting the resetting of cortical motor networks. Therefore, we have used sensorimotor oscillations, rather than event-related potentials, to investigate the intentional inhibition of voluntary actions.
Section snippets
Participants
A total of 16 participants gave their informed consent to take part in this study, with UCL ethical committee approval. One participant showed excessive blinking, and one was unable to perform the time-judgement task. The remaining 14 participants (eight females) included in the analysis were all right-handed, and had a mean age of 23.9 (SD = 5.9) years.
Procedure
The experiment consisted of 7 blocks of 40 trials each. There were two experimental conditions; “action only” and “act or inhibit”. An initial
Behavioural and perceptual results
The mean proportion of inhibition trials was 49.7% (similar to Brass & Haggard, 2007; 45.5%); there were some inter-individual differences with the proportion of inhibition trials ranging from 41.2% to 60.4%. In order to assess how participants selected between action and inhibition, we investigated the sequential pattern of action/inhibition in each participant's data. The average number of runs, defined as trials whose outcome differed from the previous trial (Wald & Wolfowitz, 1940), was 94
Discussion
Like previous studies, we found that participants could report an experience of intention, occurring some hundreds of milliseconds prior to voluntary actions (Libet et al., 1983, Sirigu et al., 2004). Moreover, participants were able to report this experience even on trials where they were instructed to prepare the action but then inhibit it at the last possible moment (Brass & Haggard, 2007). We further found that the perceived time of intention (W judgement) in action trials was earlier in
Acknowledgements
This research was supported by a Ghent University Special Research Fund (BOF) grant to MB and an ESRC grant RES-000-23-1571 to PH. PH was additionally supported by Research Fellowships from the Leverhulme Trust and the Royal Society. We are grateful to James Kilner for help and advice with statistical parametric mapping (SPM), and to Jason Musil for help with data collection. We would also like to thank two anonymous reviewers for their contributions to the final manuscript.
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