Elsevier

NeuroImage

Volume 46, Issue 4, 15 July 2009, Pages 1187-1193
NeuroImage

When doing nothing is an option: The neural correlates of deciding whether to act or not

https://doi.org/10.1016/j.neuroimage.2009.03.020Get rights and content

Abstract

The neural basis of intentionally deciding between different response alternatives has been extensively investigated and associated with the rostral cingulate zone (RCZ). However, from daily experience we know that the decision whether to do something is often prior to the decision what to do. This raises the fundamental question whether the decision to act and the decision not to act can be considered as functionally equivalent. Interestingly, in the legal domain such an equivalence is implicitly assumed by punishing crimes of omission. The aim of the current study was to explicitly test this assumption by comparing the neural representation of intentional actions with intentional non-actions. Our results suggest, that weighing whether to act or not involves similar areas of the brain, namely RCZ and dorsolateral prefrontal cortex, independent of the outcome of this decision. This finding strongly supports the assumption that intentionally not acting can be considered as a mode of action.

Introduction

Self-initiated intentional action lies at the heart of human nature. One important precondition for intentional action is the momentum of choice, e.g. the choice whether to do something or not. We are all familiar with the following situation in road traffic: we are driving along a road, we are approaching a traffic light, we spot that it turns yellow. In that moment in time we hesitate and make up our mind whether to accelerate and resume our way or not. Research on decision-making in the voluntary action domain has nearly exclusively focussed on choices between different action alternatives (Cunnington et al., 2006, Lau et al., 2004, Lau et al., 2006, Müller et al., 2007, van Eimeren et al., 2006). Deciding between different response alternatives has been associated with the rostral cingulate zone (RCZ; Debaere et al., 2003, Müller et al., 2007; Walton et al., 2004), pre-supplementary motor area (preSMA; Deiber et al., 1999, Lau et al., 2006), or both RCZ and preSMA (Cunnington et al., 2006, Lau et al., 2004, van Eimeren et al., 2006).

The more fundamental decision whether to act or not – as involved in the road traffic example – has been largely neglected. In the legal domain human societies acknowledge non-actions (namely negligence) as intentional acts by considering them as punishable under the precondition of purposefulness. This procedure implicitly assumes that the representation of voluntarily not doing something bears resemblance with the representation of voluntarily doing something. However, to our knowledge this implicit assumption has never been tested scientifically.

We set out to compare the brain areas activated during decisions whether to act or not with brain areas involved in choosing between different action alternatives. If the whether decision is associated with brain areas that have been previously associated with the decision between different response alternatives (RCZ and/or preSMA) this would support the assumption that not acting can be regarded as a response option.

We used a modified stop task (De Jong et al., 1990, De Jong et al., 1995) that bears resemblance to the traffic light example to investigate the intentional decision not to act. In a stop task participants are engaged in a primary response task (comparable to riding on a road), and occasionally and unpredictably are confronted with a signal, that instructs them to inhibit their response to the first stimulus (comparable to a traffic light suddenly changing from green to red). Since participants have to respond most of the time responding is the ‘behavioural default setting’. In order to create a condition of free choice, we modified the classical stop task by introducing a ‘decide’ signal that sometimes occurs instead of the stop signal. This signal indicates that participants can freely choose between executing the prepared action and refraining from it. After those trials participants had to indicate whether they were able to decide or whether they responded impulsively to the primary response stimulus. By subtracting brain areas involved in successful stopping from areas involved in deciding between responding and not responding we obtain a pure measure of cortical involvement in choosing to act or not to act.

According to the aforementioned considerations that voluntary non-action can be regarded as a mode of action we predict that similar brain areas should be involved in deciding to act and deciding not to act.

Section snippets

Participants

Nineteen healthy volunteers were recruited from whom we obtained written consent prior to the scanning session. All subjects had normal or corrected-to-normal vision. No subject had a history of neurological, major medical, or psychiatric disorder. The data of two subjects were excluded from the analysis one due to the lack of successful stop trials, the other due to strong movement artifacts. The remaining seventeen subjects (9 women and 8 men; age: mean = 21.6, ranging from 19 to 29) were all

Behavioral data

Overall participants responded in 3.6% of the trials erroneously. Those trials were excluded from further analysis. Mean reaction times (RTs) of the different response conditions are displayed in Table 1. Paired t-tests reveal a significant difference between RTs in the primary response and decide-go condition (t(16) =  6.27, p < 0.001). The same holds true for the comparison between the failed-to-decide and decide-go condition (t(16) =  6.90, p < 0.0001) indicating that the decision process takes

Discussion

The present study aimed at investigating the neural correlates of voluntarily choosing whether to act or not. Previous studies focussed solely on brain areas involved in voluntary action and action selection between different action alternatives (Cunnington et al., 2006, Lau et al., 2004, Lau et al., 2006, Müller et al., 2007, van Eimeren et al., 2006, Walton et al., 2004). Since we regarded the question what action to perform as secondary to the more fundamental question of whether to perform

Conclusion

Our results indicate that the brain areas involved in representation of voluntary action and voluntary non-action are virtually the same. Moreover, choosing whether to act or not to act shows a similar neural signature as selecting between different overt response options. This constitutes first evidence in favour of the current judicial procedure to regard voluntary non-actions as punishable acts.

Acknowledgment

The work was supported by the dissertation grant of the Studienstiftung des Deutschen Volkes awarded to the first author.

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