Reviews and perspectivesNeural and behavioral correlates of intentional actions
Introduction
Every human being is familiar with the concept of intentional, willed action. Yet, it turned out to be very difficult to define intentional action scientifically. To cite James, 1890, James, 1950: “Desire, wish, will, are states of mind which everyone knows, and which no definition can make plainer” (p. 486).
After this opening sentence, James, 1890, James, 1950 characterizes intentional actions in much the same way as present research still does (Brass and Haggard, 2008, Frith, 1992, Haggard, 2008, Jahanshahi and Frith, 1998), namely by contrasting them with automatic or reflex actions. James argues that, in contrast to automatic actions, voluntary actions are performed purposefully and with the intention to reach a certain goal. As a result, he reasons, an action can be performed voluntarily only if the subject has first acquired knowledge of its consequences.
In addition to being purposive and goal-directed, current definitions consider intentional actions to be endogenously controlled and stimulus-independent (Brass and Haggard, 2008, Haggard, 2008). Furthermore, they require attention and offer a choice between alternatives (Jahanshahi & Frith, 1998). They can be inhibited and are not necessarily executed once the intention to act has been formed, but can be carried out after a delay. Automatic actions, in contrast, are considered to be triggered by an environmental stimulus. They do not require attention, or only to a lesser degree, and are conducted in an immediate and stereotyped manner. Once the action program has started, automatic actions cannot be stopped and inhibited.
However, it must be noted that contrasting intentional actions with automatic actions, although very helpful for theoretical considerations, does not capture human behavior as it takes place in everyday life. Human actions are rarely totally externally determined, nor are they ever completely internally guided. Rather, they almost always comprise external and internal components. Therefore, it might be more reasonable to assume that human actions exist along a continuum between the two extremes. Considering the predominant component, actions can then be categorized into those that are more internally guided, for example, switching on the TV instead of reading a book, and those that are more externally guided by environmental stimuli, for example stopping at a red traffic light.
Moreover, voluntary action should not be considered to be a unitary concept. Rather, it comprises at least three different components: what, when and whether (Brass & Haggard, 2008). The what component concerns the decision of which action to perform, the when component the decision when to perform the action (Müller et al., 2007, Krieghoff et al., 2009), and the whether component refers to the decision whether or not to perform the action (Brass & Haggard, 2007). In the following, we will refer to the what decision as internal/external action selection and to the when decision as internal/external action timing. The terms internally/externally guided actions will be used whenever no differentiation between the what and when component is made.
The aim of the present review is to integrate research from three different domains, namely functional and structural neuroanatomy, behavioral research and psychophysiological research. While there are overview articles covering one or the other domain (e.g. Brass and Haggard, 2008, Haggard, 2008, Passingham et al., 2010), an integrative overview of all domains is still lacking.
Section snippets
Two routes to action—behavioral and EEG studies
Intentional actions have been contrasted with stimulus-driven actions not only in theoretical terms, but also empirically. The direct comparison of stimulus-based and intentional actions poses a challenge, since they differ in some central aspects. For example, stimulus-based actions are preceded by some stimulus event in the environment, whereas intentional actions by definition are not. Intentional and stimulus-based actions also differ with respect to the focus on changes in the environment,
The two routes to action hypothesis from an anatomical perspective
Twenty-five years ago based on the work of Sanides (1964) and Goldberg (1985) proposed, the existence of two distinct neuroanatomical routes to action: a medial and a lateral motor system, subserving internally and externally guided behavior respectively. Both routes converge in the primary motor cortex (M1). According to Goldberg's (1985) hypothesis, each of the two motor systems has a ‘premotor center’ the SMA for internally guided actions and the arcuate premotor area (APA) [equivalent to
Intentional actions in functional neuroimaging research
Now that we have described the neuranatomy of the mesial frontal cortex in more detail we will try to systematize brain imaging work on intentional action. In this section we combine neuroanatomical distinctions within the fronto-median wall with a functional systematization of intentional action.
Shortcomings
The aim of the present review was to provide a deeper understanding of the brain mechanisms involved in intentional action control. However, it should be noted that, in the laboratory, one has to instruct subjects to act voluntarily, a fact which is rather paradoxical but inevitable. In contrast to most situations in everyday life in which an intentional decision is associated with a certain (personal) value, there is no such value in an experimental setting. In order to have a well controlled
Conclusions
Internally and externally guided actions are at least partially controlled by different neuroanatomical networks (e.g., Goldberg, 1985). Findings from EEG studies, lesion studies and behavioral studies also support this theory. In contrast, findings from fMRI studies suggest a level difference rather than an absolute difference. One explanation for the fact that most of the fMRI studies did not show activation in the lateral network for the comparison of externally vs. internally guided actions
Acknowledgements
Florian Waszak was supported by a research grant of the Agence Nationale de la Recherche (ANR-08-FASHS-13). Marcel Brass was supported by the Special Research Fund (BOF) of Ghent University and the Bijzonder Onderzoeksfonds (BOF) of Ghent University. We thank Rosie Wallis for carefully proofreading the article.
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